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Host Manipulation by Parasites$

David P. Hughes, Jacques Brodeur, Frédéric Thomas, and Preface by Richard Dawkins, University of Oxford, UK

Print publication date: 2012

Print ISBN-13: 9780199642236

Published to Oxford Scholarship Online: December 2013

DOI: 10.1093/acprof:oso/9780199642236.001.0001

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A history of parasites and hosts, science and fashion

A history of parasites and hosts, science and fashion

Chapter:
(p.1) Chapter 1 A history of parasites and hosts, science and fashion
Source:
Host Manipulation by Parasites
Author(s):

Janice Moore

Publisher:
Oxford University Press
DOI:10.1093/acprof:oso/9780199642236.003.0001

Abstract and Keywords

This chapter reviews the history of parasite manipulation of hosts – a long history, including contributions from outstanding biologists, which was surprisingly ignored by ecologists and behavioural biologists until the early 1980s. The reasons for this shift in attitude are explored, supporting data are provided, and some other contributions to our knowledge of parasite-induced behavioural change are also covered.

Keywords:   parasite manipulation, Wesenberg-Lund, Redi, Rothschild, Cram, Wheeler, Price, Anderson, May, Hamilton-Zuk

1.1 Introduction

Not so long ago, the chasm between the study of disease and the study of ecology was so great that no one seemed able to cross it. Then again, few people tried. This is hard to understand now, but it is the way it was. Ecologists saw parasitology as something fit only for medical schools—parasites were for people in white laboratory coats, not for guys like ecologists who attended urban academic conferences kitted out by L. L. Bean, not for guys who viewed themselves as the heirs of John Audubon, if not Ernest Shackleton. Some of the folks alleged to wear white lab coats disagreed, but it was difficult for them to get a hearing, simply because everybody knew that ecology was mainly about birds and mammals, perhaps insects and plants, but certainly not about worms, much less things invisible without a microscope.

This began to change in the late 1970s, with profound effects on the study of evolution and behavioral ecology, and this book will illuminate some of those effects. My task here is to review some of the literature published prior to that sea change in what everybody knew, and I will suggest some things that might have contributed to that shift. For decades, there had been ample evidence supporting the idea that infectious organisms exert powerful evolutionary and ecological effects, but it was evidence that was largely ignored by ecologists and behavioral biologists. I will emphasize the literature around parasite-induced behavioral change; the ecology of parasites themselves also deserves something of a mention (e.g. Holmes 1961; Schad 1963; Paperna 1964; Simberloff and Moore 1997), in part because that topic has yet to attract the kind of attention that parasite–host interactions have attracted.

That said, it is difficult to understand what contributes to fashion in science. This difficulty must be compounded by the fact that, as scientists, we want to believe our own hype, which states that we are preternaturally rational and open-minded truth-seekers. Scientists are indeed those things in our better moments, but we are also social creatures, and so we tend to travel, intellectually speaking, in herds, a tendency that has been encouraged by the equally marvelous tendency of grant funding to form large clots around a small percentage of research programs. These attributes have played a role in parasite ecology, broadly defined—that is, behavioral, ecological, and evolutionary aspects of parasitism. Much like country music, there was a time when parasites were not cool, and much like country music, they are cool now.1 This is one view of how parasites came to be cool.

1.2 The days before cool

All manner of people who would not know a parasite life cycle if one bit them nonetheless know about two parasites: the worm that gets into the snail (intermediate host) and transforms its tentacles so that final host birds eat it (i.e., the trematode, Leucochloridium paradoxum and congeners) and the (p.2) worm that gets into the second intermediate host ant brain and takes control of the ant (i.e., the trematode, Dicrocoelium dendriticum and relatives). These have starred in most television documentaries and popular magazine articles about parasites and behavior, and until they recently began to share the spotlight with the even more amazing Toxoplasma gondii (and relatives), were among the invertebrates most likely to give bower birds and whales a run for their money in terms of charisma or, more likely, morbid fascination.

I will begin with L. paradoxum; unless otherwise indicated, the history I report for this trematode will be taken from Wesenberg-Lund’s delightful 1931 account of this organism, supplemented by general aspects of parasitology history as reported in Cheng (1973) and Foster (1965). Adult Leucochloridium live in songbirds; eggs pass out with feces and await consumption by snails (e.g., Succinea), where they develop into colorful, striped sporocysts that invade the snails’ tentacles. In addition to their striped appearance, the sporocysts have been observed to pulsate, especially in the presence of light.

Our knowledge of Leucochloridium begins over 200 years ago, and holds several surprises. Even the events leading to the description of the genus have a mysterious air. For instance, Kagan (1952, p. 29) tells us that in 1831, the polymath C. G. Carus reported seeing a copper engraving “of unknown origin and age” in which an infected snail was shown with eight broodsacs. (Carus went on to describe L. paradoxum in 1835.) For a while, there was some suggestion that these remarkable sporocysts might be the result of spontaneous generation. Perhaps this is not surprising, because the first trematode life cycle, that of Fasciola hepatica, was not worked out until 1881; that trematode itself had been recognized as early as 1379. It was probably much easier to believe that parasites appeared spontaneously in various tissues than to comprehend the fabulous journey that they really do make from host to host.

The notion that life could come from inanimate objects apparently held great appeal; though challenged with clever experiments beginning in the seventeenth century, it was not firmly put to rest until Pasteur’s work approximately 150 years ago. Ironically, a demonstration that fly eggs develop into maggots by Francesco Redi (he of “redia” fame) was among the first to take issue with the notion of spontaneous generation; this physician-entomologist-poet was also the first person that we know of to search through animals with the goal of finding parasites. Because of this, he is considered the founder of parasitology and the redia stage in the trematode life cycle bears his name. None of that saved Leucochloridium from spending some time, along with tapeworms, pinworms, and maggots, on the spontaneous generation list. Yet all through the history of parasitology—well before the elucidation of life cycles and Koch’s postulates—keen observers were asking if flies could transmit yaws, if mosquitoes might transmit malaria. I doubt that any of us in this post-Enlightenment world could muster the mental agility required to entertain ideas about pathogenic miasma while simultaneously considering the possibility that flies might transmit disease.

Meanwhile, the thought that parasites could increase their appeal or the appeal of their host to predators is older than we might think. For instance, C.T. Siebold (as cited in Kagan 1951) is credited with suggesting in 1853 that Leucochloridium in snails might attract avian predators, a suggestion made all the more remarkable because the first trematode life cycle awaited discovery decades in the future (see also Ahrens 1810, cited in Lewis 1977). Wesenberg-Lund (1931) reports that when he finally found an area that contained parasitized snails, he could see their swollen, pulsating tentacles from a distance of two meters. Wesenberg-Lund becomes the first, and perhaps only, person to express compassion for a trematode sporocyst: “…I confess I have been sorry for all the wasted efforts of the sacks pumping and pumping at a rate of about 70 strokes a minute” (p. 98; see Berg 1948 for more about Professor Wesenberg-Lund).

Wesenberg-Lund then presented a puzzle: “For my own part, I could have snails with Leucochloridia before my eyes for hours. The birds were singing only a few metres from them, but nevertheless I never had the good fortune to see the birds take the parasites” (p. 98). In this, he is like most of us. Despite the notoriety of Leucochloridium, few people have seen birds eat them. In part, this may be because Leucochloridium and its gastropod host are (p.3) both difficult to maintain in the laboratory and patchily distributed in nature. In part, it may be because few people today have the patience of Wesenberg-Lund.

But what of Dicrocoelium? Dicrocoelium dendriticum is nowhere nearly as conspicuous as Leucochloridium; it certainly does not visibly pulsate, nor is it striped. The adult lives in the liver of ruminants; terrestrial snails get infected with larval stages when they eat the shed eggs. The cercariae escape from the snail in masses of mucous called “slime balls,” which seem to be considered good eating by ants. It is possible to feel slightly smug that the ant—that paragon of industry and unfailing cooperation—is tempted like the rest of us by unhealthy snacks. (Dicrocoelium hospes Looss, 1907 has a similar life cycle with similar effects on the hosts; see Anokhin 1966; Romig et al. 1980 and references therein.)

The snack in question, however, is not merely unhealthy, but potentially deadly. Upon ingestion, one of the cercariae in the slime ball leaves its compatriots and encysts in the subesophageal ganglion of the ant. In the case of D. hospes, two metacercariae tend to encyst in the antennal lobes. Infected ants behave normally during the day, but at day’s end, when temperatures cool, they crawl up on blades of grass and enter a kind of torpor, often firmly seizing grass blades with mandibles, thus securing their elevated positions—positions that likely increase their vulnerability to unintentional predation by grazing ruminants. Carney (1969) described a similar phenomenon in Brachylecithum mosquensis, a dicrocoeliid parasite of perching birds, snails, and once again, ants.

The role of the ant in the life cycle of Dicrocoelium is a fairly recent discovery (Krull and Mapes 1953), and the parasite does not have the frisson associated with Leucochloridium. (“The first sight of the ‘pulsating brood-sacs’ in the tentacles of the snails is a thrilling sight to a parasitologist.” Woodhead 1935, p. 337). Nonetheless, both trematodes have captured public imagination and been grist for the mills of science writers. It is notable that neither Dicrocoelium nor Leucochloridium—both emblems of parasite manipulation—have been demonstrated to enhance their own transmission to the final host. Neither of these trematodes is well suited to experimental work, and tracking the fate of parasitized ants on a pasture is a daunting prospect.

Nematodes also entered the altered behavior/transmission story at an early stage, ushered in by Eloise Cram. She was a remarkable woman: in more than 85 years of existence, the American Society of Parasitologists has had almost as many presidents. Five of those presidents have been women, and of those, Cram was the first, in 1956 (the second, Marietta Voge, would be elected 20 years later, and the third, Lillian Mayberry, in another 20 years). Eloise Cram was, indeed, a pioneer, rising to the top of her profession, becoming a world expert first on parasites of poultry and later, on control of schistosomiasis, and leaving over 160 publications in her wake (National Agricultural Library). Early in her career, in one of these papers (Cram 1931), she observed that the larvae of the nematode Tetrameres americana cause grasshopper intermediate hosts to be “droopy and inactive, a condition which would make them easy prey for food-seeking fowls in nature.” (p. 4). The thought that parasites alter behavior in ways that could affect transmission by influencing predator–prey interactions was in the air, if one cared to notice.

Dame Miriam Rothschild did notice, as she seemed to notice most living things. Described by the New York Times (25 January 2005) as “the heiress who discovered how fleas jump,” she was fascinated by the natural world, and trematodes in snails were among the many things that caught her attention. In this respect, she was particularly interested in snail gigantism (e.g., Rothschild 1941). She noted in 1940 that there were behavioral differences in the population of Pseudosuccinea columella that she studied; snails infected with xiphidiocercariae were found on top of waterlily leaves, in direct sunlight, whereas uninfected snails were not found in such a location (Rothschild 1940, 1941a). In response to Lewis and Wright (1962), who suggested that trematodes in black flies might inhibit biting, Rothschild (1962, p. 1312) began with a statement that reflects the state of parasites and behavior at the time: “Dr. Lewis and Dr. Wright …are to be congratulated on emphasizing an extremely interesting point which has hitherto attracted little, if any, attention—namely, that infestation with larval trematodes can alter the behaviour of the (p.4) intermediate hosts”. After giving a few examples of this phenomenon, she makes one of the earliest suggestions that the behavioral alterations induced by parasites can lead to broader misperceptions about what is going on in nature, including a fair amount of sampling error: “A ‘random sample’ of specimens may prove to be only a random sample of the infested portion of a population.” (p. 1312). In this same publication, Rothschild also reports Jean Baer’s observation that the movement of sticklebacks infected with an immature stage of the cestode Schistocephalus solidus was impaired to the point of rendering them subject to capture by hand. She clearly saw parasites as players in the behavior of animals, players that had not received the attention they probably deserved.

Sticklebacks are remarkably amenable to laboratory investigation, and beginning in the 1980s, S. solidus and sticklebacks were the subject of many elegant studies aimed at elucidating all the ways that the tapeworm influenced stickleback behavior (see Moore 2002; Barber and Scharsack 2010 for reviews). Long before that, however, a related cestode (Ligula intestinalis) and its intermediate host, the roach (Leuciscus rutilus), were the subjects of the first field study to demonstrate that altered behaviors associated with parasites could result in increased predation on intermediate hosts. While examining the diet of cormorants in The Netherlands, W. H. van Dobben (1952) made some interesting parasitological observations, including the fact that while 30% of the roach taken by cormorants were infected with L. intestinalis, only 6.5% of the roach taken by fishermen were infected. Van Dobben suggested that the increased vulnerability of infected roach was the result of impaired movement.

Rothschild (1969) also noticed parasites in her beloved fleas. The way that she came to this observation was serendipitous: specifically, she found a copulating female flea on a pregnant rabbit. At first glance, without consideration of Dame Rothschild’s other work on fleas, this might not seem all that notable. Recall, however, that Rothschild and Ford (1964) reported the first case of hormonal synchronization of reproduction in parasite (flea) and host (rabbit), and so this particular flea was not supposed to be mating yet—not until it had transferred to the newborn rabbits. As Rothschild (1969, p. 10) put it, “…much to our dismay, we observed a pair of rabbit fleas copulating on the ears of a pregnant doe rabbit. We at first assumed that, somehow, we had missed this type of behaviour in the past, and that, on the quiet, some fleas were pairing on the pregnant doe…. But on less panicky second thoughts this seemed most improbable, so we fixed the two fleas and sectioned them”. The sectioning revealed that the female was host to a mermithid nematode—“coil upon coil of the parasite.” (p. 10). Rothschild was left mystified by how the female flea’s receptivity was induced, and no wonder. In over 4,000 sectioned fleas, Rothschild found only one mermithid, and that nematode was in the only prematurely copulating flea she observed. This presages what would become a rich literature on compensation for parasite-reduced fecundity, including Minchella and Loverde’s (1981) suggestion that parasitized animals facing fecundity reduction might invest more heavily in earlier reproduction.

The fact that mermithids could exert such a powerful effect on an insect host was not as surprising to Rothschild as it might have been, for she was well aware of William Morton Wheeler’s early work on mermithids in ants (Wheeler 1907, 1928). As early as 1901, Wheeler had collected highly unusual specimens of Pheidole dentatus. These were twice as long as normal individuals, and because their gasters were greatly enlarged, Wheeler estimated their volume to be 10–12x that of normal ants. These mermithergates, as he called them, each contained a mermithid nematode which, when uncoiled, was ten times the length of its enlarged host. These parasitized hosts were not only larger than their uninfected conspecifics, but they also behaved differently. They did not participate in colony tasks such as foraging or caring for brood, but instead begged for food, incessantly and voraciously.

Returning to fleas, these insects were the first hosts of parasites to reveal to investigators that altered host behavior can result in increased parasite transmission, albeit by blood-feeding vectors, not by intermediate hosts encountering predators. Bacot and Martin (1914) were remarkably understated when they said (p. 431), “…whereas certain of our fleas sucked energetically and persistently, (p.5) no blood entered their stomachs, but the oesophagus became unusually distinct”. They went on to report that dissection of these fleas revealed blocked proventriculi, and “It occurred to us that fleas whose proventriculi were obstructed with plague-culture were likely to be responsible for the conveyance of infection. ” (p. 432). By following the feeding of individual blocked fleas on rats, Bacot and Martin showed that such exposure led to a high probability of plague transmission.

Finally, in addition to their effects on host behavior, parasites were shown to alter host ecological interactions themselves. Thomas Park, who was cited by the New York Times (4 April 1992) as being “instrumental in transforming the field of ecology into a science with quantification and controlled experiments,” found that the outcome of competition between two species of flour beetle was reversed by the presence or absence of a protistan parasite (Park 1948). Typically, Tribolium castaneum competitively excludes Tribolium confusum. If the coccidian parasite Adelina tribolii is present, the outcome is reversed.

This review of our knowledge up through, say, the 1960s, is nowhere near exhaustive (see Moore 2002, for a more comprehensive review). It does not have to be exhaustive in order to support the contention that early in the development of modern biology, at least some scientists recognized that parasites could have major effects on host behavior and ecology. This recognition began with hypotheses about Leucochloridium in the first half of the nineteenth century and continued with examples from other trematodes, cestodes, nematodes, protists, and even bacteria, living in snails, fish, grasshoppers, fleas, beetles, and ants. The scientists who wondered about parasites and host behavior included some of the bright lights of their era, Fellows of the Royal Society, members of the United States National Academy of Sciences, presidents of learned societies. Casting a wider net to encompass not only behavior and what was becoming behavioral ecology, but also evolution, we see that such luminaries as J. B. S. Haldane (1949) had remarked on the potential significance of disease in evolution. This idea about parasites and how they might affect hosts was not a secret.

Nonetheless, the topic of parasitism, be it in the broad areas of ecology or evolution, or the developing study of animal behavior, was largely ignored. As Haldane (1949, p. 68) put it, “When however an attempt is made to show how natural selection acts, the structure or function considered is almost always one concerned either with protection against natural forces such as cold or against predators, or one which helps the organism to obtain food or mates”. In other words, pathogens and parasites did not enter the picture.

This was certainly the world that I found as a graduate student. Because my personal experience encompassed the shift from the world that rejected the behavioral/ecological/evolutionary study of parasite–host interactions to the world that accepts it, I am going to take a brief detour here and describe my personal experience—not because I am somehow special, but because the scientists who didn’t live through this era might find it otherwise hard to believe. I had first heard of parasites changing behavior as an undergraduate, when I had the good fortune of studying parasitology at Rice University under the tutelage of Clark Read, acknowledged as one of the more creative thinkers and teachers the field has seen. Read allocated the critical nuts and bolts of parasitology—the identification, diagnosis, and life cycles—to the laboratory, and spent the lecture time pacing the floor, sharing the mysteries of the field and posing thought experiments. One of the mysteries that made its way into Read’s classroom was Holmes and Bethel’s now classic work on acanthocephalan-induced behavioral alterations (Holmes and Bethel 1972; Bethel and Holmes 1977 and references therein). I had never heard of such a thing, and I was intrigued—by the magic of the life cycles, by the highly derived structures (all those hooks and suckers!), and now by the ability of these animals to seemingly reach out and transform the lives and activities of other animals. I informed Read that I wanted to study parasites and how they affected behavior. He told me that no one was doing much of that kind of research, but that if I got a strong foundation in parasitology and animal behavior, I could certainly put it together myself. In retrospect, I am amazed by his optimism and grateful for my own response to it, however naϯve.

(p.6) I followed Read’s advice, and completed a Master’s degree focused on insect behavior. I then decided to add parasites to the mix, and looked for a doctoral program where I could do that. The struggle to get a hearing as a graduate student who was interested in parasites and host behavior was an education in itself. Both ecologists and behavioral biologists informed me that parasites had very little to do with their own disciplines and that I should study what they were studying, not parasites. I decided to take some time away from degree programs and found employment as a technician with a truly remarkable scientist, Lynn Riddiford; during that time, I probably learned more about how to conduct science and how to conduct myself as a scientist than I did in any other two years of my professional life. When I returned to school, I understood how to develop an independent research program, and I found a department populated by scientists who were perfectly willing to question what everybody knew, and to believe that if we could study behavior and ecology with birds, we could do it with worms! The University of New Mexico was not rich, but it offered graduate students small research grants to pursue independent projects. It was the perfect setting to study parasites and host behavior.

Of course, there was the nagging thought that this was a temporary respite, that I would finish my degree and the great world of biology would respond with yet another collective yawn when I trotted out my dissertation about parasites and host behavior (see Moore 1983, 1984). Luckily for me, about the time that I finished that dissertation, the scientific world began to change.

This change didn’t happen overnight, of course. It had been building for a while. For instance, clever ecologists and evolutionary biologists had been eyeing parasitic castration, offering evolutionary explanations for this widespread phenomenon, a trait of parasites that were possibly having their cake (a living host) and eating it, or at least some of it, too (e.g., Kuris 1974; Baudoin 1975). In addition, stories of altered host behavior had continued to surface. William Bethel and John Holmes (1973, 1974, 1977) had matched van Dobben’s field demonstration of altered host behavior resulting in enhanced predation on intermediate hosts, producing their own clear and elegant laboratory confirmation of the same phenomenon, this time using gammarids infected with acanthocephalans and exposed to duck predation. They categorized types of alterations and made ecological predictions about predator/final host traits that would favor each type. Rothschild’s observations of gastropod behavior altered by trematodes were confirmed by other scientists (e.g., Sinderman and Farrin 1962; Lambert and Farley 1968). Questions arose about the possibility of host suicide as an adaptation to parasitism (Shapiro 1976; Smith Trail 1980) and about the evolutionary history of altered behaviors (Szidat 1969). Following the work of Bacot decades earlier, medical entomologists began to find that feeding and flight in biting flies were dramatically affected by all manner of parasites (reviewed in Moore 1993). And off in the world of insect pathology, ignored by not only ecologists and behavioral biologists but also parasitologists, reports of summit disease caused by viruses and fungi continued to pile up. Indeed, when we consider the vast number of ecological studies carried out on organisms like ants and gastropods, animals whose abundance and distribution can be profoundly affected by whether or not they have certain parasites, and when we consider how many of those studies do not acknowledge the possible existence of parasites, much less estimate their levels, the idea that some truths are inconvenient takes on additional meaning.

1.3 Becoming cool

There was indeed an accretion of evidence supporting the fact that parasites have ecological, evolutionary and behavioral significance, but that might have gone unnoticed for quite a while longer were it not for three endeavors that I view as primarily responsible for shifting the attention of ecologists and evolutionary and behavioral biologists toward parasites. They address different areas of parasite evolutionary biology and ecology; their combined effect was a sea change in how other organismal biologists viewed parasites.

Traditionally, parasites were thought to evolve toward a benign coexistence with their hosts; this (p.7) was an idea widely accepted and taught in the medical community. It had been questioned on occasion (e.g., Ball 1943), but the doubt had not penetrated the seemingly common-sense certainty that supported the idea: killing one’s dwelling and food source (host) did not appear to be a particularly adaptive thing to do. Beginning in the 1970s, Roy Anderson and Robert May (1991 and references therein), began to question the conventional wisdom about how parasites evolved, especially when it came to their effects on their hosts. They did so by returning to a fundamental concept in evolution and population ecology—that of fitness, one measure of which can be expressed as reproductive rate (R0). They examined microparasites and macroparasites, that is, parasites that are relatively small and that have short life spans, during which they reproduce within the host, and parasites that are somewhat larger, live longer, and whose offspring exit the host and colonize new hosts. Microparasites tend to induce stronger immune responses than macroparasites do, and this in turn affects the likelihood of reinfection.

Of course, May and Anderson knew that the biological reality of parasites did not segregate so neatly, but the distinction worked well for the purposes of their models, which in their most streamlined forms addressed reproductive rate in terms of host population density, host recovery rate, and host death rate from parasites (virulence) and from other causes. One of the many outcomes of their work, and perhaps one of the most relevant for the study of manipulation, is that traits like life history, resource use, and transmission can greatly influence virulence. For instance, consider transmission: if virulence is linked to that trait in such a way that transmission increases with virulent infections, then if all else is equal, virulence will be favored by natural selection, that is, reproductive rate will increase. This means that given the complexity and diversity of host–parasite associations, there is no single roadway to virulence or avirulence, there is no one-size-fits-all statement about how parasite–host associations should evolve; instead, the diversity of host–parasite interactions produces countless possibilities. Anderson and May’s work planted the study of how hosts and parasites interact squarely in the middle of evolutionary theory, causing science and medicine to see the evolution of sickness and health in a different light.

Peter Price entered the world of parasite ecology and evolution from the vantage point of a forest entomologist. Having done extensive research on sawflies and parasitoids, he was impressed with the vast array of organisms that might be considered parasitic, what they had in common, and the extent to which all of this was underappreciated. Some of this he attributed to historical anthropocentrism that saw “mammals and birds, and particularly man …[as] the glories of the evolutionary process”. (Price 1980, p. 13). This same vision shuttled parasites down “blind alleys”.

In contrast to this view, Price wrote a book for the Princeton Monographs in Population Biology (Price 1980), introducing it with the following sentence (p. 3): “Parasites form a large proportion of the diversity of life on earth”. Price explored definitions of the word “parasite” (always a slippery prospect), and expanded its traditional application, noting that most of an individual parasite’s food comes from a single organism. As a result, his parasite could be any one of a number of organisms taken from an array not unlike the passenger manifest for a Noah’s Ark of Very Small Things—from leafhoppers to beetles to bugs (and beyond), as well as the usual culprits that populate parasitology books. Much like a colonial explorer stepping onto an uncharted continent—but with a much greater understanding of what he might be getting into—Price courageously laid claim to well over half of the world’s living creatures as appropriate objects of study for those interested in parasites (see also Price 1975, 1977 for the earliest explorations of this theme). From these, he extracted some ecological and evolutionary commonalities (e.g., small size relative to host, high rates of evolution and speciation, high potential for adaptive radiation and sympatric speciation). This, in turn, led most notably to explorations of phylogeny and community ecology (Holmes and Price 1980) and parasite-mediated host interactions (Price et al. 1986).

Bill Hamilton had been interested in the relationship between disease and sexual reproduction for some time (e.g., Hamilton 1980). In 1982, he and (p.8) Marlene Zuk presented what became their eponymous hypothesis to explain the fact that in many species, males have traits associated with courtship that are conspicuous in behavior and/or appearance (Hamilton and Zuk 1982). They hypothesized that such showiness can only be sustained by a healthy male, one that is resistant to parasites, and that in preferring males with such traits, females are selecting males with resistant genes. The hypothesis predicts that within a species, females should prefer males with lower parasitemia; across species, those species that are subject to the highest levels of parasite attack should demonstrate the most conspicuous sexually selected traits.

Behavioral ecologists sprang into action; the eagerness to test this hypothesis produced something akin to a stampede in some quarters, and the resulting literature is still being plumbed. Behavioral ecologists and evolutionary biologists began to discover some things that immunologists and parasitologists had known for quite some time, such as linkages among hormones, stress, and the immune system.

Of course, memory is notoriously fickle, so I decided to “test” my sea change hypothesis—that parasites and host behavior became fashionable in eco-evo-behavioral circles around 1980, when May and Anderson, Price, and Hamilton and Zuk published their ideas. I used the bibliography of Moore (2002) as a source of publications in the field. This bibliography is fairly comprehensive and was compiled for purposes other than examining historical trends; it ranges widely and deeply, to say the least, for in my reading and writing I honestly attempted to leave no stone unturned. In the analysis for this chapter, after dismissing a number of references that were from collections, edited volumes, and the like, along with some papers that were irrelevant to this question, I allocated each of the remaining publications cited in Moore (2002) to one of three groups based on journal type as reflected in journal title: parasitological (including medical, pathology, N = 417), ecological/evolutionary/behavioral (N = 277), and general (e.g., physiology, entomology (and other “-ologies,”), Nature, Science, PNAS; N = 441). I did not use papers published after 1999, as these were newer at the time the bibliography was generated, and therefore more subject to unintentional drift into one area or another that might bias the current analysis. I then asked how articles about parasite–host interactions sorted within these groups across decades: What proportion of articles in each of the three groups was written in each decade? The results, shown in Table 1.1, support the

Table 1.1 Percentage of scientific papers containing information about parasite–host interactions that pertain to host behavior in each of three categories of journals, sorted by decade of publication.

Decade of publication

Parasitology*

General**

Behavior/Ecology***

N = 417

N = 441

N = 277

1990s

42.9

32.9

67.1

1980s

32.6

31.3

23.1

1970s

11.7

17.5

6.1

1960s

7.7

9.5

2.2

1950s

3.1

4.5

1.1

1940s

<0.5

1.4

<0.5

1930s

0.7

1.4

0

1920s

<0.5

0.7

0

1910s

<0.5

0.9

0

(*) “Parasitology” category journals were those with some references to parasites, pathology, veterinary or human medicine, and the like in their titles.

(**) “General” category journals were largely those devoted to broad categories of science or to organismal studies.

(***) “Behavior/Ecology” category journals were largely those that are devoted to behavioral, ecological, or evolutionary studies.

(p.9) observation that there was a decided increase in parasitology-related interests among ecologists and evolutionary and behavioral biologists later in the twentieth century. Of course, there are many sources of potential bias in such an analysis, ranging from the varying birth rates of different types of journals to my own sorting rules, however straightforward I tried to make them. Nonetheless, the sudden and belated recognition of parasites in ecological/behavioral/evolutionary circles shows in the fact that of all the papers with parasitological content published in that category of journals, 67% of them were published in the 1990s (compared to 43% for parasitology-oriented journals and 33% for general journals during that time period). Put another way, out of 143 cited papers published in the 1970s, 12% were published in the “ecology” group journals; that increased to 18.9% of 338 in the 1980s and doubled to 36.5% of 510 in the 1990s.

These three influences, then—the work of May and Anderson, Price, and Hamilton and Zuk—seemed to be the starting point for a new look at parasites in the world of behavioral ecology and evolution. In introducing his book, Peter Price said (p. 3), “Indeed, I think there is much room for recasting the image of parasites held among biologists, and in so doing, certain views in ecology, evolutionary theory, and biology must also be recast”. That process has begun.

1.4 Beyond manipulation

Finally, there is the fact that not all altered behaviors benefit the parasite. Parasite benefit was the focus of much early work in parasites and host behavior, perhaps a lingering influence of the visual drama around Leucochloridium. It continues to command attention, as investigators address possible mechanisms and seek ways to explain its evolution. Although parasite benefit is implicit in the word “manipulation,” as if the parasite is a puppeteer, there are times that behavior is altered by parasites in ways that benefit the host. The first examples of this were in the area of parasite avoidance—especially the avoidance of and defense against biting flies—and because these studies were often sequestered in the medical entomology literature, they received little attention from ecologists and other non-entomologists. Edman’s work in particular ranged across the 1970s and 1980s (Edman and Spielman 1988 and references therein). As time went on, other ways to avoid parasites, especially those having to do with mate choice, captured the attention of a wide range of biologists.

Even if an animal gets infected, there are behavioral changes that occur that can benefit the host instead of the parasite. These behaviors range from self-medication to grooming, but some of the earliest observations were around homeostasis, and in particular, behavioral ways to regulate body temperature in animals that could not do so metabolically. For instance, in 1974, Vaughn and co-workers showed that desert iguanas responded behaviorally to an injection of a pyrogen (in this case, killed pathogenic bacteria), increasing their body temperature by 2 oC. Matthew Kluger did much to raise awareness of fever as an adaptive response (e.g., Kluger 1986; 1991). Some of the behaviors displayed by parasitized animals that seem to be a result of manipulation leading to increased predation risk (e.g., conspicuous behavior, elevation seeking, hyperactivity, positive phototaxis, etc.) might have originated with fever responses (Horton and Moore 1993; Moore 2002).

Given this background, it remained for Benjamin Hart, a professor of veterinary medicine, to introduce the idea that the constellation of behaviors associated with febrile sickness was not evidence of debilitation, as traditionally thought by the medical community, but was instead adaptive (Hart 1988). These behaviors are consistent across host taxa, type of pathogen, and disease severity, and are typified by anorexia, sleep, “depressed” behavior—in other words, behaviors that redirect resources toward combating the pathogen. At the time Hart suggested this, behavioral biologists had become more interested in the effects that parasites had on animals, but they were still not terribly interested in the behavior of animals that were simply “sick”. Instead, they assumed that sick animals were abnormal, and therefore not suitable for study. Hart’s background in veterinary medicine may well have been crucial to his ability to see the behavior of sick animals in a way that had escaped other behavioral (p.10) scientists. In so doing, he, along with others, helped create a conceptual counterweight to the purely manipulative (parasite benefit) explanation for altered host behavior. Hart has also synthesized much of the literature on grooming behavior as an adaptive measure (see also Clayton 1990), and has worked extensively on the antibacterial activity of saliva, that is, the wisdom of licking one’s wounds (e.g., Hart and Powell 1990).

There is at least one more aspect of the study of parasite–host interactions that intrigues me. When parasites were first becoming cool, women were still rare in scientific circles. Because of this, I have found it pleasantly puzzling that so many women seemed to gravitate toward the study of parasite–host interactions, specifically those with a greater or lesser behavioral twist. In addition to myself, there are at least eight women that I can think of who were beginning their careers during this 1980-ish era. That is a lot of women during a time when many entire departments had no women faculty members, or perhaps one token female; that is a lot of women in a field that itself was not so large. I have sometimes speculated about why this happened, but I lack testable hypotheses. What I can do is briefly introduce these women; they are creative scientists and good people, well met (see Box 1.1). (In addition, the field seemed to gain more traction among UK and UK-trained scientists than in the United States, but that may be a topic for another chapter!)

1.5 Conclusion

I am thankful that this history has no real conclusion, at least not in the sense of “ending”. I am (p.11) fairly certain that parasites, including manipulating parasites, will be cool for the foreseeable future, and that they provide remarkably fertile subjects for study. We still have much to understand, including fundamental questions about genetic bases of manipulation, geographic variation in host–parasite interactions, and evolutionary antecedents of manipulation. Indeed, the list seems without end. Moreover, having studied parasites when they were not cool, and then when they were, I am fairly convinced that cool is better.

I am not sure, however, that this leap into coolness—the trend that became apparent in the 1990s-is cause for unfettered celebration. Some reflection is in order: here in this book, we have a collection of chapters about phenomena that might have been dismissed as irrelevant three decades ago. Given the increasing costs of research and diminishing resources, how likely is it today for the next uncool field to emerge into the spotlight? What do we all lose when fashion—what “everybody knows”—closes the door on what might be discovered? I suspect we lose more than information, as precious as that is. We lose some of the creative impulse, the angle that no one else has noticed, the patient, delighted watchfulness of Wesenberg-Lund.

So in the midst of celebrating what we have learned about manipulative parasites, I suggest that we also remember that just recently we were intellectual refugees. With such a heritage, we should of course savor what we are doing—and we should keep watching, peering into dark, neglected corners for the next thing that everyone knows is not very cool.

Acknowledgements

I am grateful to the editors of this volume who invited me to participate, who gave me permission to write this sort of piece and even encouraged it, and who were remarkably patient when other writing commitments played havoc with my schedule. I am grateful to David Hughes in particular for suggestions, comments, and encouragement. I thank John Holmes, the doyen of this field, for taking time out from an active retirement in order to give me valuable feedback on an earlier draft.

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(p.14) Afterword

John Alcock

Janice Moore asks many intriguing questions about parasites and behavioral research in her chapter on the prehistory of the modern field of parasite-influenced animal behavior. The two that I wish to comment on here are: (1) why were researchers so slow to catch on to the possibility that a great deal of animal behavior is profoundly influenced by parasite pressure? (2) Is the current interest in the field of behavioral parasitology a result of a bandwagon effect, with modern researchers hurrying to cash in on the latest fashionable topic before the funding moves to a new hot topic?

At the heart of these questions is the reality that behavioral biologists have only relatively recently become interested in the evolutionary consequences of interactions between microscopic parasites and their hosts. I am representative of this group of latecomers to the topic. In the first edition of my textbook, Animal Behavior, An Evolutionary Approach, published in 1975, I did describe how avian brood parasites afflicted their victims, but microscopic parasites received nary a mention. Not until the fifth edition, published in 1989, did the textbook deal briefly with the issue of the possible effects of debilitating microparasites on the evolution of animal behavior.

And yet, as Moore points out, stunning examples of parasite-induced changes in animal behavior were well known long before the more recent surge of interest in parasitology. For example, she describes how, ever since the 1930s, biologists were familiar with the amazing case of a trematode parasite that induces a snail to make sporocyst-infected tentacles resemble worms, the better to lure worm-eating birds to eat the tentacles and ingest the sporocysts. Yet this and other similar accounts had little effect on the field of animal behavior. It was not until the 1980s that parasites suddenly became a hot topic for behavioral types, a phenomenon that Moore traces to the ecological work of Peter Price and a paper by William Hamilton and Marlene Zuk. In their paper, Hamilton and Zuk argued that blood parasites and the like had affected the evolution of female mate choice in birds with colorful plumage. Hamilton and Zuk proposed that the feathers of some male birds had properties that permitted females to evaluate the parasite load carried by a potential partner, the better to pick a healthy, non-infectious partner or perhaps even parasite-resistant male able to pass on his good (anti-parasite) genes to the female’s offspring.

These studies marked the beginning of the era when it became “cool” to study microscopic parasites. Now it could be that others stampeded after Price and Hamilton because these persons were well-established, highly successful researchers from whom others took their cues about how to succeed in science. (Zuk was just beginning her fine career in 1982.) There is little doubt that Hamilton and Zuk’s paper did catch the imagination of many, myself included. Their paper was featured in my fifth edition and in every subsequent edition to the present. But if the enthusiasm that I, as a textbook writer, and others, as behavioral researchers, had and have for this paper happened because of a bandwagon effect, we still have to explain why Hamilton and Zuk were able to get the bandwagon rolling whereas earlier studies of parasitic life cycles did not do so.

Let me suggest why parasitological studies in the earlier part of the twentieth century failed to generate (p.15) much interest in microparasites by behavioral biologists at the time. This work, astonishing though the complex parasite–host interactions were, was nonetheless primarily descriptive with little or no theoretical foundation, ecological or evolutionary. In this, parasitologists at the time were not fundamentally different from the ornithologists, mammalogists, entomologists, herpetologists, ichthyologists, and other -ologists who dominated biology departments then. As George C. Williams demonstrated, by the mid-1900s, almost all biologists had forgotten the essence of Darwinian logic and were prone to explain adaptations in terms of their supposed benefits to the species as a whole. Williams’s book, Adaptation and Natural Selection, published in 1966, helped biologists rediscover the point that evolutionary change by natural and sexual selection occurs when individuals, not entire species or groups within species, differ in their hereditary ability to produce surviving descendants. Williams, along with W.D. Hamilton, Richard Alexander, and Robert Trivers, demonstrated just how productive this fundamental idea could be for studies of animal behavior. Hamilton and Zuk’s paper was one more powerful demonstration that you might be able to explain the adaptive value of certain traits in novel, testable ways—if you really understood evolutionary theory.

The development of an “adaptationist programme” by Williams and its popularization by Richard Dawkins (in The Selfish Gene, published in 1975), encouraged all sorts of biologists to understand Darwinian evolutionary theory. This in turn made possible the explosive development of an entire discipline, behavioral ecology, of which behavioral parasitology is now one component. At the time this was happening, some researchers complained that the new breed of behavioral biologists were giving way too much attention to evolutionary studies at the expense of those focused on the immediate, proximate causes of behavior. But this complaint ignored the fact that, prior to the evolutionary revolution initiated by Williams, researchers had largely failed to properly investigate the adaptive basis of behavior, which had nothing to do with preventing the extinction of species or groups. The shift to modern behavioral ecology was largely compensatory for this earlier failure. Thanks to Williams, and later Hamilton and Zuk, we know now that evolutionary theory is immensely helpful in moving beyond natural history, important though descriptive natural history is. The complex life cycles of certain minute parasites are wonderful to know about, but it is also valuable to consider how a female tanager’s criteria for mate choice may have evolved because of variation among the males of her species in their susceptibility to invisible microparasites. What a cool idea.

Notes:

(1) “I Was Country when Country Wasn’t Cool” –a song by Kye Fleming and Dennis Morgan, made popular by American country singer Barbara Mandrell in 1981—which was about the time parasites began to be seen as cool.