General considerations

One unifying characteristic of most organisms is their ability to distinguish entities of their own bodies from entities that are genetically different. This ability to distinguish ‘self’ from ‘non-self’ originated in the deepest roots of the Tree of Life, when natural selection favored individual prokaryotes that could phagocytize potential food and not kin or potential mating partners. Likewise, sexual reproduction, another unifying characteristic on almost all branches of the Tree of Life, requires the recognition of appropriate gametes. The processes underlying recognition of self/non-self are undoubtedly complex, as we will see, but they fundamentally require intimate, molecular-level interactions at the interface (usually on cell surfaces) between two unrelated partners. Herein lies the foundation of one of the key processes that defines biological systems: cell–cell communication, and the ability for all organisms to protect themselves from potential invaders, both abiotic and biotic, via immunity.

In the introductory chapter, we alluded to the phenomenal success of the parasitic way of life. In a sense, this success should not surprise us. Individuals that adopt a life style that avoids predators and diseases, that provides access to potentially limitless resources, that provides access to mates, and so on, should be favored by natural selection. Yet, all organisms that adopt this life style confront the constraint of avoiding (or limiting) immunological defenses (and other host defenses, see Chapter 16), many of which can drive parasite reproductive success to zero. Thus, the host immune response represents a critical selective force on individual parasites. As we will see later in this chapter, and throughout this book, the manner in which parasites evade the sophisticated host immune response has major consequences to human health and to the development of parasite control strategies.

General considerations

The protists (Greek, the very first), also referred to as the protozoans (Greek, protofirst, zoaanimals), comprise a spectacular diversity of unicellular, eukaryotic organisms possessing organelles such as a membrane-bound nucleus, mitochondria, chloroplasts, Golgi, etc., found in the metazoan plants and animals. There is considerable evidence that eukaryotic protists evolved by a process of sequential endosymbiosis of prokaryotes (see Box 3.1, as well as Margulis (1981) for a discussion of the theory). The Kingdom Protista was erected almost 150 years ago by the famous German zoologist Ernst Haeckel in an attempt to accommodate this diversity. Today, with considerable ultrastructural, genetic, and biochemical research and the molecular phylogenetic revolution, it is now known that unicellular animals are distributed among all kingdoms. There is no longer a formal taxonomic category called the Protista. However, ‘protist’ is still widely used as a general term (as is ‘protozoan’) when referring to this diversity of unicellular eukaryotes, even though neither of these terms implies monophyletic origins.

Within the confines of a single cell membrane (= plasmolemma), these organisms have undergone an enormous adaptive radiation. This single cell functions as a complete organism. Protists are not simple; they feed, move, behave, and reproduce, and, thus, can be considered more complex and versatile than our own cells! Complexity arises from the specialization of organelles. Protists have evolved a bewildering array of morphologies, physiologies, behaviors, reproductive strategies, life histories, and nutritional and locomotory modes. In short, the diversity of protist form and function rivals that encountered among all other animals combined.

General considerations

The pentastomids (Greek, pentafive, stomamouth), or tongue worms, are a small group of obligatory parasites that includes about 130 species. The taxonomic name was erroneously coined in the belief that each of the hooked appendages that flank the true mouth had a mouth. Some species supposedly resemble a miniature vertebrate tongue. Adult pentastomids are found primarily in the respiratory passages of terrestrial vertebrates, mostly reptiles. They range in size from a few millimeters to 15 cm in length. Approximately 70% of the definitive hosts for pentastomes are snakes; several pentastome species have also been described from lizards and freshwater turtles and crocodilians. Relatively few adult pentastomes have been described from amphibians, birds, or mammals, although some species are reported from such unusual sites and hosts as the air sacs of marine birds, the trachea of vultures, and the nasopharynx and sinuses of canines and felines. Raillietiella is the most speciose pentastome genus and is the only one known to mature in amphibian hosts. The unique site specificity of pentastomes, coupled with their hematophagus feeding habit, large body size, and long-lived nature have inspired fascinating studies in parasite ecology and evolution (review in Riley, 1986). Particular focus has been on examining the mechanisms by which these large parasites evade their vertebrate host’s immune response (reviews in Riley, 1992; Riley and Henderson, 1999; see Box 10.1).

In this second edition, we stay true to the philosophical approach that was adopted in the first. Thus, we continue to see a need for a single text with dual focus on the diversity and ecology/evolution of parasites. At the core, we feel that an ideal strategy for senior undergraduate and beginning graduate students to understand and appreciate breakthroughs in parasite ecology is through a solid understanding of parallel advances in parasite diversity, life-cycle variation, systematics, and functional morphology. By way of example, we suggest that an understanding of the role of falciparum malaria in determining the worldwide distribution of the human sickle-cell gene, and thus the role of parasites in mediating natural selection (Chapter 16), comes from an understanding of life-cycle variation, functional morphology, and biodiversity of the apicomplexans (Chapter 3). Likewise, real understanding of the evidence in support of the parasite hypothesis for the evolution and maintenance of sexual reproduction in molluscs (Chapter 16) comes from a detailed understanding of variation in life cycles and life histories of the platyhelminths (Chapter 6). This dual focus, under one cover, is the hallmark of this text.

Our aim is to provide students with a synthetic understanding of the biodiversity, ecology, and evolution of animal parasites. Thus, throughout most of the text, we unabashedly take a parasite-centered view of the phenomenon of parasitism. Yet, we also aim to provide insights on the nature of the host–parasite interaction itself. It is for this reason that following a brief introductory chapter, we provide an overview of vertebrate and invertebrate immunity, and the new discipline of ecological immunology. We turn again and again to the importance of fundamental immunological principles throughout the text.

General considerations

Parasites comprise the most significant component of our planet’s biodiversity, and are integral components of all ecosystems, often playing pivotal ecological and evolutionary roles. We hope you have been convinced by previous chapters that, for example, parasites may influence the biology of their hosts in a myriad of ways. Many parasites manipulate the phenotypes of their hosts dramatically. Some parasites have been shown to also regulate host populations. Others can impact the evolution of their hosts and act as powerful agents of natural selection. Parasites can mediate the competitive interactions between free-living animals and act as ‘cryptic determinants of animal community structure’ (Minchella & Scott, 1991). It is not surprising that concepts such as ‘keystone parasite’ and ‘ecosystem engineer’ have been applied to parasitic animals, alluding to their significant ecological roles in nature (e.g., Thomas et al., 1999; see Chapter 15). Indeed, there is increasing evidence that, paradoxically, the ‘healthiest’ ecosystems are those which are rich in parasites, due to their influence on a range of ecosystem functions, their important roles in food web structure and function, and as ‘drivers’ of biodiversity (reviews in Marcogliese, 2005; Hudson et al., 2006).

In addition to these diverse ecological and evolutionary roles, recall that parasites are also widely studied from an applied perspective, e.g., as biological tags in fisheries stock management (see Chapter 14), and as indicators of complex food web interactions (e.g., Marcogliese & Cone, 1997a). This chapter reviews yet another contribution of parasites, as posed by Lafferty (1997), “What can parasites tell us about human impacts on the environment?”

Encounters with parasites

On a fateful spring day in a small northern Canadian town in the 1970s, two of the authors (the two that are related) of this text came upon a sickly red fox. Following some foolhardy thinking, they handled the fox and carried it home. A few days later, health officials diagnosed the fox with rabies. To avoid the fatal consequences of the disease, the brothers required daily intramuscular injections of the prophylactic drug that was used at the time. We recall the episode with memories of pain, dismay from parents, and ruthless teasing from our friends. And so goes our introduction to the world of parasites. So too goes our introduction to the phenomenon of parasitism. Readers might envision two teenagers discussing how their predicament arose: How did that fox get infected? Why was the fox population, but not the racoon population, so heavily infected that year? How does the virus migrate from the site of a wound, to the brain, to saliva? How, and why, does it transform a normally secretive and nocturnal animal into one that is aggressive and diurnal? There are obvious parallels between these early queries and modern questions associated with host specificity, parasite site selection, the geographical mosaic of coevolution, and mechanisms of alterations in host behavior.

General considerations

The common name of the nematomorphs, ‘horsehair worm’ or ‘hairworm,’ arises from their long filariform, cylindrical morphology. Adult body size among the approximately 350 described species varies considerably, ranging from a few centimeters in length to over 2 m. Nematomorphs are dioecious and the large adults (Fig. 9.1) are free-living in aquatic habitats, mostly permanent freshwater lakes, ephemeral ponds, and streams. In contrast, juvenile nematomorphs are obligate parasites within the hemocoel of arthropods, a characteristic they share with the mermithid nematodes (see Chapter 8). The juveniles of almost all described nematomorphs are parasitic in terrestrial arthropods (the gordiids), whereas the remainder (the nectonematids) are parasites of marine invertebrates, especially crustaceans. Nematomorphs are often referred to as gordiids or Gordian worms on account of the tangled mass of swarming adults (Gordian knots) that are frequently observed in shallow aquatic habitats. Compared to the mermithids and their potential for biological control of insect pests and vectors, the nematomorphs are a poorly studied group. Following the first completion of a nematomorph life cycle under laboratory conditions (Hanelt & Janovy, 2004b), significant advances have been made in our understanding of the ecology, systematics, and life cycles of this enigmatic taxon (review in Hanelt et al., 2005). The facilitation of nematomorph transmission between its parasitic larval stage and its free-living adult stage in water is now a well-known case of parasite-induced alteration in host behavior (see Chapter 15, Color plate Fig. 8.3).

General considerations

Following decades of taxonomic upheaval, strong molecular phylogenetic evidence now indicates that the phylum Microspora is a monophyletic lineage within the Kingdom Fungi (review in Corradi & Keeling, 2009). Members of this clade are obligate, intracellular, spore-forming parasites. The unique and distinctive spores of these unicellular eukaryotes are minute, ranging from 2 to 20 µm in length. Although they are eukaryotic, microsporidian cells have several unusual characteristics, including a lack of organelles such as flagella, peroxisomes, mitochondria, and Golgi apparatus. Microsporidians also have 16S rather than 18S ribosomes. However, despite their relative simplicity, they can also be considered as marvels of structural and functional complexity, possessing adaptations for survival while outside their host, and also for intracellular parasitism. Within the spore is a diagnostic, exquisite extrusion apparatus, adapted for the penetration of host cells.

Louis Pasteur described the first microsporidian in the mid nineteenth century. He showed that Nosema bombycis caused ‘pebrine disease’ in silk-moth larvae, and provided recommendations to European silkworm farmers regarding control. Currently, a total of approximately 1300 species of microsporidians in 160 genera have been described. Following from modern advances in molecular diagnostics, it is likely that many more species await discovery. While most microsporidians are parasites of insects, they infect a wide range of other invertebrates, including nematodes, molluscs, annelids, and crustaceans. Microsporidians are present within all five classes of vertebrates, with 14 genera described from teleost fishes alone. Research involving microsporidians has traditionally focused on economically important species of insects (e.g., Nosema spp., review in Wittner & Weiss, 1999) and fish (e.g., Loma spp., review in Dyková, 2006). In recent years, this focus has expanded to include microsporidians that have been implicated as causative agents of opportunistic infections and emergent diseases in humans (review in Weiss, 2001).

General considerations

The lesser scaup, Aythya affinis, is a common duck of the western North American prairies. Even the etymology of its genus name, Aythya (=water bird) suggests it is an unremarkable species of duck. Yet, for parasite ecologists it is far from unremarkable. In a classic study of parasite biodiversity, Albert O. Bush counted almost 1 000 000 parasites in a sample of 45 scaup, representing an astonishing 52 species of gut helminths alone (Bush & Holmes, 1986a, b). Although parasite biodiversity of this magnitude was foreshadowed by earlier studies on bird–helminth interactions by the fathers of parasite ecology in the former Soviet Union (Dogiel, 1964) and Poland (Wisniewski, 1958), Bush’s work was the first to rigorously quantify the occurrence and intensity of individual species within individual hosts. His study was also the first to place parasite communities into the conceptual framework of mainstream community ecology.

We highlight the scaup–helminth example to emphasize a point that lies at the heart of parasite community ecology, i.e., individual hosts almost always contain more than one species of parasite. This basic tenet prompts several intriguing questions. Do the species compete for limiting resources and then assort themselves in a non-random manner to reduce interspecific overlap? Does the presence of one species impose fitness costs on co-occurring species? Do species assort themselves to increase the probability of intraspecific mating or to avoid interspecific mating? Are biodiverse parasite communities less likely to be invaded than depauperate communities? Similar questions can be asked at different scales. Why, for example, is parasite biodiversity higher in scaup than in other species of bird, even sympatric ones with which they share bodies of water? What is the role of host phylogeny versus host ecology in determining interspecific variation in parasite biodiversity? It is questions such as these that have inspired parasite ecologists since the earlier studies by Dogiel and Wisniewski. Such questions provide the framework for this chapter.

General considerations

We now shift our attention to the geographical distributions of parasites. Although spatial aspects of parasite distributions were considered in the previous chapter, our focus here is on parasite distributions at broader scales, typically on the order of continents or regions. This perspective is the realm of parasite biogeography. In general, biogeographers aim to characterize patterns in the geographical distribution of organisms and to understand the role of historical events in determining present-day distributions of populations, species, and entire biotas (Brown & Lomolino, 1998). This fundamental aim seems straightforward, but the subject matter of biogeography is notoriously complex. Modern studies in biogeography combine aspects of phylogenetics, ecology, geographical information sciences, paleontology, and geology to understand present-day distributions, and to reconstruct the sequence of events leading to the assembly of faunas in space and time. For parasite biogeographers, the task is especially complex, and interesting, because understanding parasite distributions requires an intimate knowledge of the ecological and evolutionary factors that determine the distributions of all of their hosts.

For convenience, biogeographers recognize two broad research traditions. Historical biogeographers seek to understand the origin, dispersal, and extinction of species relative to geological events such as continental drift, glaciation, and the emergence and submergence of landmasses. A key paradigm that underlies historical biogeography is the notion that the geographical range of a species, or an entire biota, can be split into isolated parts by physical barriers to dispersal or gene flow (e.g., the isthmus of Panama, the Beringia land bridge) that results in the formation of sister species or sister faunas. This research arm is known as vicariant biogeography. In contrast, ecological biogeography tends to focus on the extent to which the distributions of species result from current ecological processes.

General considerations

The Nematoda (Greek, nemathread), or roundworms, are perhaps the most abundant and diverse group of multicellular animals on earth. Free-living nematode densities can exceed over 1 million individuals per square meter in some shallow-water marine sediments. Furthermore, free-living nematodes exploit a greater array of ecological habitats than any other metazoan. Many are significant detritivores or decomposers that play a disproportionately large role in recycling chemicals and organic nutrients in aquatic and terrestrial ecosystems. Others feed on bacteria and other microorganisms and are important in food web relationships. Approximately 20 000 nematode species have been described. However, it is certain that this is an underestimate of total biodiversity, with perhaps as many as one million species. The difficulty in describing nematodes, in part, is related to their small sizes and their notorious uniformity in internal and external morphology. However, it is clear that their small sizes and cylindrical, tapered shapes have contributed to their extraordinary adaptive radiation within diverse ecosystems, as well as their exploitation of both plants and animals as hosts.

Nematodes are typically dioecious, exhibit sexual dimorphism, and vary in size from 1 mm to well over 1 m in length. The world’s largest nematode species is the massive Placentonema gigantissima in the placenta of sperm whales; female worms are approximately 8 m long! Nematodes have a fluid-filled pseudocoelom and are bilaterally symmetrical. All possess a complex multilayered cuticle that is molted four times before reaching sexual maturity. Like the acanthocephalans, nematodes also exhibit eutely whereby most adult tissues are composed of a constant number of cells and growth is due to increased cell size rather than an increase in cell number. Adults possess a complete, but simple, digestive system. Their reproductive systems are also relatively simple, but their life cycles are exceptionally varied.

The ability of parasites to cause disease has always been an important reason to study them, and the teaching of parasitology has almost always been stimulated by conditions conducive to disease, such as war or climate change. Currently, zoonotic diseases emerging from altered ecosystems, or carried by arthropod vectors spreading their ranges due to climate changes, supply that stimulation. However, most of us who teach, or have taught, parasitology have chosen that topic because of the fascinating life cycles of many parasites and their complex interactions with their hosts. Much of that fascination stemmed from learning how parasites can affect the population dynamics of their hosts, or the behavior of the hosts, or even the evolution of their hosts. In addition, that fascination was based on how much parasites could tell us about the life of their hosts, such as their diet, travels, or evolution. Or even of the earth itself – some of the earliest evidence for continental drift was the similarity in parasites of amphibians in Africa and South America. Examples of all of these influences are provided in this book.

Many of the systems that parasitologists have used to show these fascinating features have become relatively easy to study due to new techniques, such as those in genomics and proteomics, which have provided new and more powerful ways to study systematics, evolution, and host–parasite relationships. This has attracted the attention of biologists with a wide variety of backgrounds, so that much of the very interesting work done on host–parasite systems recently has been done by those trained in other specialties, such as ecology, behavior, neurophysiology, and evolutionary biology. Very few of the students in senior-level parasitology courses will go on for further study in parasitology, but many more will go on for further study in other biological specialties. Our courses, books, readings, and other materials used in our classes should be chosen to expose those students to the usefulness of parasites in investigations in their chosen fields.

General considerations

Our previous chapters focused on the functional morphology, life cycles and ecology of a wide range of animal parasites. One of our aims in these chapters was to highlight the complexity and fascination of the parasitic life style. Another was to introduce the idea that the seemingly infinite diversity of parasite life cycles and adaptations could be interpreted under an ecological umbrella. Armed with this background knowledge, we now consider unifying principles of ecology and evolution that can be applied to the phenomenon of parasitism.

We begin our transition with a consideration of the complex nature of parasite populations and the general ecological characteristics of the individuals that comprise them. We highlight the nature of enquiry at this level by first considering two examples. In a field survey, Cornwell & Cowan (1963) monitored the transmission of gut helminths into 180 canvasback ducks, Aythya valisineria, sampled from a small wetland in western Canada. The authors controlled for sampling heterogeneity by restricting their collections to ducklings within individual clutches. Their results showed that even within a single clutch, individual siblings harbored between 90 and 6000 worms! In another field survey, Valtonen et al. (2004) censused adult acanthocephalan populations in individual ringed seals, Phoca hispida, collected from the Baltic Sea. Although the collections spanned a 22-year period when the seal and intermediate host populations varied extensively, the prevalence of acanthocephalans was always 100% and the mean number of worms fluctuated within a single order of magnitude. Thus, on the one hand, mean parasite infrapopulation sizes can vary tremendously, even within very narrow spatial and temporal scales. On the other hand, population sizes can be remarkably stable, barely fluctuating around an equilibrium value. Characterizing this extreme variation at both narrow and broad temporal and spatial scales and understanding the underlying mechanisms that determine it are the central objectives of parasite population ecologists and ecological epidemiologists.