Modification of host behavior and transmission in the acanthocephalan Acanthocephalus dirus: effects of development, intraspecific conflict, and host sex
Date of Award
Master of Science (MS)
Timothy Sparkes, PhD
Kenshu Shimada, PhD
Stan Cohn, PhD
Parasites are organisms that live on or in another in order to survive. In some cases, parasites require more than one host to complete their life cycle and rely on a predation event for transmission to the next host. Inside the host, the parasite must access host resources to grow and develop from the non-infective to infective stages. At the infective stage, the parasite is able to survive within the definitive host. Development to this stage has been correlated with changes in antipredatory behaviors, body size and color, and reproduction of intermediate hosts in ways that may increase predation by definitive hosts. However, these changes may not always be adaptive manipulation by the parasite, and may be the result of pathological responses to infection, or a counter-adaptation of the host. If host modification is adaptive for the parasite, then the timing of these changes should occur when the parasite is capable of surviving in the definitive host.
Acanthocephalan parasites have been commonly associated with changes in host phenotype after infection. Early summer, the parasite Acanthocephalus dirus infects the stream-dwelling isopod Caecidotea intermedius as its intermediate host. Throughout the fall and winter, the parasite develops from the non-infective (acanthellae) to the infective stage (cystacanth) inside the isopod. During this time, changes in isopod refuge use behavior, activity, body color, and mating responses have been associated with infection by A. dirus. In the spring, parasites are then transmitted through predation to definitive hosts, green sunfish (Lepomis cyanellus) and creek chub (Semotilus atromaculatus), where they can complete their life cycle. The relative synchrony of this system may give insight into host manipulation as an adaptive strategy for parasites.
This was one of few studies that evaluated the relationship between A. dirus and its hosts using a field-based approach. The isopod and fish surveys were conducted every month for 12 months, between 2016 and 2017. Isopods were collected from a stream in Lake County, Illinois, and information about refuge use, host sex, body size, and infection status were recorded. Individuals of A. dirus were recovered from isopods and measured, sexed, and developmental stage was determined. Fish hosts were collected using seine nets, and were later measured and examined for parasites. Isopod and parasite data were later combined with data from previous surveys.
I examined pre-existing differences in refuge use behavior by comparing refuge use in infected and uninfected isopods during early stages of infection. I found that pre-existing differences were present but they were unlikely to influence behavior patterns seen during late-stage infection.
I assessed the relationship of parasite development as a predictor of refuge use, and found that the pattern of refuge use modification was sex-specific. In males, parasite development was related to changes in refuge use behavior, which indicated that development to the cystacanth stage was associated with timing of modification. Thus, changes in refuge use appeared to be adaptive manipulation by parasites in male hosts. In females, parasite development was not related to changes in refuge use behavior, which indicated that development to the cystacanth stage was not related to changes in refuge use behavior. It is possible that size constraints present only in female isopods affect the timing of refuge use modification, so that parasite development is indirectly related to changes in host behavior. However, this may still be explained by other hypotheses.
One potential explanation for sex-specific differences is that female isopods are naturally smaller than males and may allocate energy towards reproduction over growth. Thus, parasites within females may be more constrained than in male hosts and may need to modify host size before growth and development can occur. Consistent with this explanation, I found that infected females were larger than uninfected females, and this was not due to pre-existing differences in size. I also found that infected males were larger than uninfected males, but this may be explained by pre-existing differences in size. However, analysis of parasite growth showed no effect of host sex on parasite body size.
I also examined the potential for conflict between infective and non-infective parasites within hosts, and this was also sex-specific during the time period examined. In females, there was no difference in the level of refuge use behavior between acanthellae-only and cystacanth-only infections, and thus, there was no potential for conflict. In males, there was a potential for conflict, and mixed-stage infections indicated that non-infective parasites may sabotage manipulative effects of mature parasites when sharing a host.
Lastly, I used measures of behavior modification and prevalence of parasites in fish hosts to determine the overall pattern of modification and transmission. I found that behavior modification was highest in the spring, and that the onset of these changes coincided with the occurrence of parasites in fish hosts. The results indicated that behavior modification is likely an effective strategy for transmission. Further analysis showed that patterns of transmission were also sex-specific. It is likely that male isopods provide conditions for parasites that are unconstrained in energy and space available for growth, and are transmitted to fish sooner in the year relative to females. Thus, parasites infecting fish during the fall months likely originated from a male isopod, and are more likely to have higher fitness payoffs than parasites in females.
Teemer, Sara R., "Modification of host behavior and transmission in the acanthocephalan Acanthocephalus dirus: effects of development, intraspecific conflict, and host sex" (2019). College of Science and Health Theses and Dissertations. 328.