Parasite-host co-evolution has resulted in complex adaptations, many of which lead to modifications of host behavior or fitness. Parasites can be pathogenic to hosts, introducing adverse effects that cause morbidity or mortality (Christensen 1978, Beach et al. 1985, Koella et al. 2002, Valkiūnas and Iezhova 2004, Valkiūnas et al. 2014, Gutiérrez-López et al. 2019b, Yang et al. 2019, Adams et al. 2021). In other relationships, parasite infection of vertebrate hosts can result in modified behavior (Lafferty and Morris 1996), or have no observable effects on host biology (Ashby and Boots 2015). Vector-borne pathogens, which respond to adaptive pressure from both vertebrate and arthropod hosts, are no exception; parasite-induced alterations in vector behavior and biology can significantly influence parasite transmission (Hacker and Kilama 1974, Hogg and Hurd 1997, Gutiérrez-López et al. 2019b). Vectorial capacity is a framework describing all the intrinsic and extrinsic factors that contribute to an arthropod vector’s ability to transmit pathogens, including survivorship, vector competence, and number of infective bites (Kramer and Ciota 2015). Parasite-induced modifications of host-seeking activity or flight activity may increase (or decrease) the number of infective bites delivered to naïve hosts or alter survivorship by augmenting the magnitude of high-risk behaviors, thus changing vectorial capacity by increasing mosquito survivorship. Mosquito flight is a risky behavior that may lead to increased mortality in mosquito hosts. By modifying the flight behavior of its mosquito host, Plasmodium parasites can guarantee sporogenesis, and increased probability of transmission.
Although malaria parasites (Plasmodium spp.) are responsible for one of the most detrimental human diseases, the impact of these parasites on some aspects of their mosquito hosts remains unclear (Cator et al. 2012, Santiago-Alarcon and Ferreira 2020). Prior studies demonstrate Plasmodium parasites can alter mosquito survivorship, feeding behavior, and even fecundity indicating that these parasites are generally detrimental to mosquito fitness (Koella et al. 1998, Anderson et al. 1999, Koella et al. 2002, Lacroix et al. 2005, Cornet et al. 2013a, b, 2019). However, in some scenarios, these parasite-induced modifications can benefit the transmission of Plasmodium parasites. For example, Vezilier et al. (2012) demonstrated that although mosquito fecundity was decreased in Culex pipiens mosquitoes infected with Plasmodium relictum (lineage SGS1), mosquito survivorship was increased (Vézilier et al. 2012). This suggests that parasites divert reproductive resources within the mosquitoes to extend their survivorship.
Locomotion is fundamental to mosquito biology as they obtain nutrients required to survive and reproduce. Therefore, a reduction in flight in a mosquito may have negative consequences on their survival or reproductive fitness. Prior studies have identified a reduction in flight activity after infection with a pathogen. Berry et al (1987) found that the filarial nematode Dirofilaria immitis significantly reduced Aedes aegypti flight activity eight days after infection with the parasite. Similarly, Rowland and Boersma (1988) found flight activity in Anopeheles stephensi mosquitoes was reduced by approximately 33% 17 days post-infection with Plasmodium yoelii parasites. A variety of parasite taxa have been shown to alter mosquito flight activity, but few studies have attempted to quantify flight activity post-infection with Plasmodium parasites due to its challenging nature. These data enhance our ability to accurately predict disease transmission or implement vector-borne disease preventions in areas with high Plasmodium transmission.
The effect of Plasmodium parasites on the behavior of mosquito hosts has been explored in several studies with conflicting results (Santiago-Alarcon and Ferreira 2020). Koella et al. (1998) demonstrated alterations to Anopheles gambiae mosquito biting behavior that would improve the transmission of Plasmodium falciparum parasites, including an increase in multiple biting events (Koella et al. 1998). Other studies have shown that vertebrate hosts infected with Plasmodium spp. are more attractive to both infected and uninfected mosquitoes, suggesting that the parasites are altering the host-seeking behavior of the mosquitoes (Cornet et al. 2013a, b, Díez-Fernández et al. 2020). However, other studies have demonstrated no effect on the attractiveness of mosquitoes to Plasmodium-infected vertebrate hosts, or that it is dependent on the intensity of infection (Yan et al. 2018, Gutiérrez-López et al. 2019a). Modifications to mosquito-host attraction by Plasmodium parasites can have important ramifications for transmission and warrants further study.
Avian Plasmodium spp. (avian malaria) provide a model system to study the effects of parasite infection on the behavior of their mosquito hosts. Avian malaria lineages are closely related to human Plasmodium parasites and have a cosmopolitan distribution (Valkiūnas 2005, Bensch et al. 2009). Because of this, many studies utilize avian malaria parasites to study vector-parasite interactions to contrast relationships in multiple systems. Here we quantify the flight activity of Culex quinquefasciatus mosquitoes infected with the avian parasite Plasmodium relictum (GRW4 lineage).