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Changes in the morphology, physiology, and behavior of parasitized organisms provide an ideal opportunity to examine the extended phenotype of parasites. Because the quality of the host directly affects the fitness of the parasite, parasites may increase their fitness by manipulating phenotypes of low-quality hosts. Males are usually preyed on by females in sexual cannibalism. Thus, the males of sexually cannibalistic species are unsafe and low-quality hosts for parasites, whereas females may be beneficial hosts because of the chance of nutrient intake from cannibalized males. Under passive modes of transmission, parasites cannot choose the host sex. Such parasites exploiting sexually cannibalistic organisms are subjected to contrasting fitness effects and may evolve to manipulate host mating behavior in a sex-specific manner: decreasing male mating to avoid cannibalism and promoting female mating to engage in cannibalism. We examined this hypothesis by a behavioral experiment using a mantid–hairworm system. Parasitized male mantids (Tenodera angustipennis) changed their behavior as expected, exhibiting increased escapes and decreased courtships and mountings, potentially avoiding encounters with the female. Interestingly, male attack behavior was promoted, possibly decreasing contact with the encountered female. However, contrary to our prediction, parasitized females also exhibited decreased propensities of mating, suggesting costs or little benefits of host mating for parasites in the female host. This study provides novel insights into the evolution of parasite strategies in response to sexual differences in host quality.
Changes in the morphology, physiology, and behavior of parasitized organisms provide an ideal opportunity to examine the extended phenotype of parasites. Because the quality of the host directly affects the fitness of the parasite, parasites may increase their fitness by manipulating phenotypes of low-quality hosts. Males are usually preyed on by females in sexual cannibalism. Thus, the males of sexually cannibalistic species are unsafe and low-quality hosts for parasites, whereas females may be beneficial hosts because of the chance of nutrient intake from cannibalized males. Under passive modes of transmission, parasites cannot choose the host sex. Such parasites exploiting sexually cannibalistic organisms are subjected to contrasting fitness effects and may evolve to manipulate host mating behavior in a sex-specific manner: decreasing male mating to avoid cannibalism and promoting female mating to engage in cannibalism. We examined this hypothesis by a behavioral experiment using a mantid–hairworm system. Parasitized male mantids (Tenodera angustipennis) changed their behavior as expected, exhibiting increased escapes and decreased courtships and mountings, potentially avoiding encounters with the female. Interestingly, male attack behavior was promoted, possibly decreasing contact with the encountered female. However, contrary to our prediction, parasitized females also exhibited decreased propensities of mating, suggesting costs or little benefits of host mating for parasites in the female host. This study provides novel insights into the evolution of parasite strategies in response to sexual differences in host quality.
Mermithidae and Nematomorpha are parasitoids united by the commonalities in their lifestyle – immature stages infect arthropod hosts, species from both phyla can manipulate their host to induce a similar water-seeking behaviour, and both have a final free-living non-feeding adult reproductive stage, often killing their host upon emergence. Some of these species are of great economic importance, being evaluated as biological control agents against mosquito vectors responsible for diseases like malaria, and other insect pests, but with scarce genomic resources currently available. Nematomorpha, despite being closely related to Nematoda, received insufficient attention in genomic research, leading to gaps in our understanding of their diverse genetic makeup. This study aimed to investigate the genetic features encoded in the genomes of both parasitoid taxa to identify similarities and parallels linked to their ecological lifestyles. We performed a comparative analysis of 12 genomes, comprising parasitoid, parasitic and free-living worms. The investigation revealed genomic signatures unique to parasitoid species, including expanded gene families enriched in neural transmission modulation, likely linked to the known host manipulation that both mermithids and nematomorphs exert on their hosts. The analysis also uncovered a diverse array of conserved transposable element superfamilies across both lineages. The findings from this study provide valuable insights into the potential genomic adaptations associated with parasitoidism in nematode and nematomorph worms. The identification of expanded gene families and conserved transposable element superfamilies sheds light on the molecular underpinnings of their unique biological traits. Additionally, the core set of orthologs specific to parasitoid worms offers new avenues for understanding the evolution of parasitism within these groups of organisms.
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