Host Behavior Manipulation by Parasitic Insects and Insect Parasites

Host Behavior Manipulation by Parasitic Insects and Insect Parasites Rustie Robison Department of Bioagricultural Sciences and Pest Management April 8, 2009 RustieLRobison@gmail.com Abstract Insects and parasites are ubiquitous. In any environment, there are numerous insects and parasites. Independent evolutionary selection has occurred and parasites and insects are taxonomically diverse (Roy et al, 2006). However, many insect-parasite interacts have evolved between insects and parasites due to the number and habitat overlap of the groups (Roy et al, 2006). In addition, to the separation of the groups there are insects that have evolved to be parasites. Over the course of evolutionary time these parasite-host interactions have resulted in numerous modifications of the insect host including morphology, behavior, and physiological by many methods. The behavior of the insect host is modified, often to the benefit of the parasite. However, these relationships are not always negative. There are numerous examples of hostparasite interactions that are mutualistic. Introduction General Overview of Host-Parasite Relationships Parasitism is a type of symbiotic relationship between two different organisms. The relationship is often one-sided and the parasite uses the host for resources. A parasitoid is a type of parasite that usually has only one host for the completion of the life cycle and the host is usually killed (Cole et al, 2002). There are many types of relationships in the host-parasite 1

interactions. The host-parasite paradigm has and continues to be a puzzle in the hands of researchers and scientists. The arms race of the host and parasite, including the evolution and selection, is an enigma. Independent evolutionary selection has occurred on taxa of parasites and insects resulting in taxonomic diversification (Roy et al, 2006). However, many interacts between these two groups have evolved, due to the sheer number and habitat overlap (Roy et al, 2006). These interactions may lead to an evolutionary arms race between the parasite and its insect host (Hoffman et al, 2008; Rolff et al, 2001, Ives, 1995). In addition, these interactions lead to many questions. How do parasites and their insect hosts interact and communicate? How do parasites control insect behavior? Even though there are many unanswered questions, parasites controlling host behavior is a widespread phenomenon. Parasites cause a whole suite of changes in host behavior, physiology, and morphology (Poulin, 1998). Both parasites and parasitoids alter the physiology and the behavior of the host (Cole et al, 2002). There are many reasons for the alteration of host behavior. These reasons range from simple pathology to more complex selection of the population (Poulin, 1998). Many studies on manipulation of host behavior by parasites have been conducted. The diversity and abundance of both insects and microbes, as well as the similarity of habitats, has lead to insect and microbial symbiotic relationships (Roy et al, 2006). In addition, the abundance and diversity of insects has also lead to the commonality of insects being parasitized by other insects. Insects are continuously affected by insect parasites and parasitic insects. Host behavioral manipulations are commonly caused by both insect parasites and parasites of insects. Insect parasites include microbial organisms such as fungus and bacteria. Insect parasites include numerous other organisms such as protozoans, insects, and nematodes, to name a few. These parasitic insects can be divided into endoparasitic (internal) or exoparasitic 2

(external). External parasites include organisms such as ticks, mites, insect larvae such as wasps, and other organisms. External parasites are not as much as an influence on host behavior because the hormone and immune system are not in direct interaction with the parasite. Endoparasitic, internal, parasites are much more influential on behavior of the host due to the intimate interaction with host immune and endocrine systems (Caldera et al, 2009; Beckage, 1985; Beckage, 1991; Cole et al, 2002; Truman and Riddiford, 2002; Poulin, 1998). In current research the endocrine system is the major factor in the defense, regulation, and control of parasites (Libersat et al, 2009). Endoparasitic insects and parasites usually develop in the hemocoel of the infected insect host (Beckage, 1985; Gross, 1993). The hemocoel of the insect is where the regulation of hormones occurs (Beckage, 1985). These types of interactions involve endocrine changes that are mediated by the hemocoel where developmental, behavioral, and metabolic signals are transported to regulate behavior changes (Beckage, 1985; Cole et al, 2002). In this paper the endoparasites, those that feed internally, will be the focus. These changes occur at a genetic level, which affect the organism and potentially the population. How does parasitism affect selection? Many of these changes involve individual behavior variation due to manipulations of the nervous system directly, or by indirect changes in the endocrine and immune systems hormones or metabolism changes. The function of the parasitized insects in populations, communities or ecosystems will be altered due to changes in foraging, sexual behavior, behavior, communication, and activity levels (Caldera et al, 2009; Beckage, 1985; Beckage, 1991; Cole et al, 2002; Truman and Riddiford, 2002; Poulin, 1998). These changes have large scale consequences on processes of natural selection and evolution. Not all host-parasite interactions are negative; there are examples of symbiotic relationships between host and parasite. Certain ant species (Formicidae: Hymenoptera) engage 3

in obligatory mutualism with fungi. The research is continuous in this complicated field. The mechanisms of host manipulation by insect parasites and parasitic insects are being researched extensively. (a) Camponotus ant with Hirsutella emergence from cuticle (b) Cricket (Memobius sylvestris) with hairworm (Tellinii spinochordes) emerging (c)ampulex compressa stinging a cockroach (Periplaneta americana) Figure 1: The images show general types of fatal interactions between parasites and insect hosts. Reproduced from Libersat et al, 2009 Parasitic Insects There are many groups of insects that act as parasites on other insects. Most notably are the order Hymenoptera, specifically the wasps. These wasps are highly evolved to be parasitoids. Though the wasps are parasitoids of many species, many of the parasitoids are specialists. These specialist wasps have co- evolved with their host and an interaction has developed over time. Wasps are very common as parasites of other insects. In fact, 4

Hymenoptera are one of the most diverse groups of parasitic insects (Whitfield, 1998). Hymenopterans live in nearly all habitats, terrestrial and aquatic and fill ecological niches, including pollinator, predator, and parasite (Whitfield, 1998). There are many examples of wasp parasitism of insect hosts. Libersat et al (2009), describes the process of envenomization of a cock roach (Periplaneta americana) by Ampulex compressa (see figure 1 & 2). This envenomization affects the walking-related behaviors of the roach (Libersat et al, 2009). Figure 2: This image represents the current model of the neurophysiological effects induced by envenomization of cockroaches by Ampulex compresa (see figure 1 for image of envenomization of the cockroach) Reproduced from Libersat et al, 2009. 5

The wasp parasitoid s venom is inserted into the cerebral ganglia which controls the thoracic movements, including walking patterns. Inhibition is the result and the roach is not able to escape using normal escape patterns (Libersat et al, 2009). If the wasp does not inject the venom into the correct location the cockroach will be unaffected. Therefore, Libersat et al (2009) addresses the question of how envenomization can be so selective. The answer is related to the venom targets that are for specific pathways, specifically for the control of the escape response. The escape response is related to the success of the wasp offspring and the overall fitness. The selectiveness of the interaction is important in the survival of the parasitoid (Libersat et al, 2009; Gross, 1993). Once the cockroach has been injected with venom the wasp parasitoid can deposit the egg into the host for further development. The egg will hatch and the larvae will continue to grow within the cockroach until it reaches maturity and kills the roach by escape, or outgrowing the cockroach host. The processes that occur during the development of the endoparasite life stages will be discussed later in the paper. In addition to wasps, numerous other insects are parasites of other insects (see appendix A). These include many families in the Hymenoptera, Diptera, and Strepsiptera. For example, Compsilura concinnata (Diptera: Tachinidae) parasitizes a Lymantriidae caterpillar, Lymantria dispar (Beckage, 1985). These endoparasites are developmentally synchronized with their hosts endocrine systems in order to ensure success of the parasite offspring. Insect Parasites There are also many groups of insect parasites including bacteria, viruses, fungus, nematodes, and other insects. Most notably fungal insect relationships have been studied by numerous researchers. Roy (2006) states that fungi are common parasites of arthropods. There 6

are about 700 known species of Entomopathogenic fungi (Roy et al, 2006) (see figure 3). Many of these parasitic fungus may have an alternative host in order to complete the life cycle, often the alternative host of the Entomopathogenic fungus is another insect (Roy et al, 2006). Figure 3: Life cycle of an entomopathogenic fungi, Entomophthora muscae in Delia radicum. (Reproduced from Roy et al, 2006) Blanford and Thomas (2001) noted that in the desert locust, Schistocerca gregaria it became infected with a fungus, Metarhizium anisopliae var acridum. Arthurs and Thomas (2001) also noted that in the field, locusts and grasshoppers were observed to be infected with Metarhizium anisopliae var. acridum, the same fungal entomopathogen. Arthurs and Thomas (2001) reported the pathogen increases the susceptibility of the host to predation. To test this field observation a laboratory experiment was conducted and the results show that infection with Metarhizium anisopliae var. acridum does cause behavioral changes that effect survivorship of the locusts (Arthurs and Thomas, 2001). In a related paper, Metarhizium anisopliae var. acridum was associated with behavioral fever in acridids (Blanford and Thomas, 2001). This change in 7

behavior by increasing preferred body temperature is associated with host searching of new microclimates that are beneficial for the parasite (Arthurs and Thomas, 2001). Mechanisms of Behavior Modification Induced by Insect Parasites and Parasitic Insects The effects of the parasite on the insect host behavior can be direct or indirect (Libersat et al, 2009). Direct manipulation of host behavior is often associated with nervous system modification. The indirect manipulation of behavior is more often associated with host endocrine and metabolism (Libersat et al, 2009). The endocrine system in an insect host is responsible for the production and regulation of hormones. In addition to hormone production and regulation, the endocrine system maintains growth and development, as well as, physiological function. Manipulations of host behavior by both insect parasites and parasitic insects include increases in temperature (behavioral fever), feeding behavior changes (consumption and location), reproductive behavior changes, and social behavior (Roy et al, 2006; Moore, 1995; Arthurs and Thomas, 2001; Poulin, 1998; Beckage, 1985). The American cockroach (Periplanta americana) is frequently infected with Monofiliformis moniformis. This infection by the parasite species causes erratic behavior changes when the cockroach is in high light situations. The cockroach will move toward the light and will become hyperactive as well (Moore, 1995). There also been many phylogenic approaches to try to understand the unique relationships between insect parasites and parasitic insects and their insect hosts. Poulin (1998) found that changes in the manipulation of host behavior may be related to phylogeny. This would make sense from a evolutionary sense if a specific behavior is a host or a parasite adaption (Poulin, 1998). Many of these behavior traits are thought to have evolved independently, in 8

many diverse insect hosts and parasites (Poulin, 1998). Poulin (1998) notes that two distinct taxa develop similar juvenile and adult life cycles even though they are not related in lineage; these life cycles are noted to cause very similar behavior manipulation of the host. Parasitism and the manipulation of host behavior has evolved independently over time (Poulin, 1998). Behavioral Fever When the body temperature of an insect host is increased to levels above normal due to the presence of a parasite this is termed behavioral fever (Roy et al, 2006; Arthurs and Thomas, 2001). This increase in the body temperature outside the normal range is a common response to a parasite invasion, especially a fungal parasite. The production of heat is energetically costly and may not be effective in ridding the host of the parasite but it has been shown to delay mortality of the insect host (Roy et al, 2006). In Musca domestica, a house fly, experiments were conducted to monitor fever of the fly when it was infected with Entomophthora schizophorae (Roy et al, 2006). The results of the experiments do indicate that higher temperatures are preferred in the house flies that are infected with the parasite (see figure 4). Any insect species that can regulate body temperature has the possibility of retaining normal behavior and inhibiting parasite growth (Roy et al, 2006; Arthurs and Thomas, 2001). 9

Figure 4: The images show general types of interactions between parasites and insect hosts. (Reproduced from Libersat et al, 2009 10

Feeding Behavior Host feeding behaviors are often manipulated by parasites. The consumption and the location of the feeding are shown to be affected by the presence of insect parasites and parasitic insects in the host (Roy et al, 2006). When the dose of the parasite is high, there is a reduction in feeding this is due to a reduction in digestive abilities by the host (Roy et al, 2006). In addition, some insects will change feeding locations. This location change may be a dispersal mechanism for the parasite (Roy et al, 2006). There is very few studies that have tried to address the question of feeding behavior changes in parasite infected insect hosts. Reproductive Behavior A very important behavior in all insects is the reproductive behavior. Reproductive behavior can be very specific in some insects and more general in others. Regardless of the specificity the reproductive behavior ensures lifetime fitness and reproductive success. Any modifications to this system could have enormous consequences for the fitness of an insect. Resources for reproduction can be diverted to the parasite (Roy et al, 2006); this alternative allocation can reduce fecundity of the insect host (Roy et al, 2006; Poulin, 1998). Roy et al (2006) suggest this may be an effect of reduction of juvenile hormone, though experimentation is needed to prove that statement. In addition, sex pheromones may be changed. Roy et al (2006) note that female moths that were infected with Z. radicans significantly reduced sex pheromone production. The reproductive behavior and the pheromone behavior may be altered when an insect is parasitized. 11

Social Behavior Many aspects of social behavior may be affected by insect parasites and parasitic insects. Ants are a complex social group. The introduction of a parasite could be detrimental to the entire colony. A whole suite of behaviors are noted in social and eusocial insects including increased grooming, cleaning, antibiotic production, removal of infected individuals. Avoidance is another behavior to ensure against parasites, individuals can avoid parasites and the colony can be moved to avoid pandemic parasitic infection (Roy et al, 2006). It is common in many eusocial colonies to remove the dead. In red fire ants, the individuals that are infected with B. bassiana are buried (Roy et al, 2006). The density of the colony makes it highly susceptible to parasite invasions. The constant grooming and tidiness of the colony will reduce the chances of parasite infection. The behavior of the colony is dictated by the altruistic behavior of the individuals. If these behaviors are manipulated by insect parasites or parasitic insects then the whole colony would be in jeopardy. More research is needed to understand the interactions of eusocial insect-parasite dynamic and to detect possible evolutionary consequences of parasite infection. Defensive Reactions Taken by the Parasitized Host There are numerous strategies that are utilized to defend against parasites. Many of these strategies involve the same behavioral changes that are induced by the parasite itself (Roy et al, 2006). In addition, these defensive strategies can be broad spectrum or a very specific response much like the response seen in plants to pathogens. 12

Insect Symbioses Not all insect-parasite interactions are detrimental to the host and have a negative connotation. There are numerous examples of symbioses between an insect host and a parasite. Many insects, such as termites and cockroaches utilize microbes for digestion of food (Caldera et al, 2009). Other insects utilize microbes for aiding in the growing of food. These fungusgrowing ants (Formicidae), the leaf-cutters, use manure to grow fungus. The fungus is then applied to the hyphal tips which allow enlarged food structures much like our own agricultural practices of fertilizer addition (Caldera et al, 2009). Evolutionary Consequences Though many questions remain numerous studies are being conducted to answer the complicated questions about insect-parasite dynamics. The questions are big in scale and relate to the future of both the parasite and the insect host. Where will the co-evolutionary arms race take the involved individuals? How does this shape reproduction of the insect and the parasite? What other long term consequences? Conclusions Many of the behavioral changes associated with insect parasites and parasitic insects may be determined by changes in the endocrine system, directly or indirectly (Beckage, 1991; Roy et al, 2006; Gross, 1993). There are many areas of research that are focusing on the interaction between insect hosts and parasites. The field of Insect Parasitology is broad and many questions still remain in the enigma of the host-parasite interaction. Independent evolutionary selection has occurred and parasites and insects are taxonomically diverse (Roy et al, 2006). However, 13

many interacts have evolved between insects and parasites due to the number and habitat overlap of the groups (Roy et al, 2006). In addition, to the separation of the groups there are insects that have evolved to be parasites. Over the course of evolutionary time these parasite-host interactions have resulted in numerous modifications of the insect host including morphology, behavior, and physiological by many methods. The behavior of the insect host is modified, often for the benefit of the parasite. However, these relationships are not always negative. There are numerous examples of host-parasite interactions that are mutualistic. Many of these interactions, as previously mentioned, involve eusocial ants which are at a higher risk for parasite infection and would have larger number of fitness and evolutionary consequences. In turn, the ants have evolved to utilize the potential fatal pathogen and to direct aspects of the fungus to food production. Insects and parasites are ubiquitous. The numbers and the diversity of insects and their remarkable adaptation to all terrestrial and freshwater niches have allowed for enormous diversification. Along with this great diversification, come many questions that will need to be addressed in future research and experimentation of both insect parasite and parasitic insects and their interactions with the insect hosts. 14

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Appendixes Appendix A Developmental synchrony between endoparasites and their hosts (Reproduced from Beckage, 1985) 17

Appendix B Summary of Endocrine Effects of endoparasitism on insect hosts (reproduced from Beckage, 1985) 2