BRANTA — Jiayue Yan
Ecology of Vector-Borne Diseases: Effects of Host Traits on Mosquito Feeding Preferences and Its Implications for Disease Transmission
Institution: EBD-CSIC/University of Seville
Supervisors: Jordi Figuerola, Laura Gangoso, Josué Martínez-de la Puente
Details: PhD, 2017
Avda. Américo Vespucio 26, Seville E41092, Spain
Subject Keywords: Insect Ecology, Insect Ethology, Ornithology, Animal Parasitology
Species Keywords: House Sparrow, Passer domesticus, Culex pipiens, Culex restuans
Last decades have seen an accelerated emergence or re-emergence of vector- borne diseases (VBDs) in many geographic areas, representing a major threat to public health and biodiversity conservation involving human, wildlife and domestic animals. Despite the medical and economic impact of VBDs, the ecology of VBDs, especially the interaction between hosts and vectors is still poorly understood. Previous studies on epidemiology assumed a random host-vector interaction and ignored the potential effects of heterogeneity in host traits, such as individual ́s health status and evolutionary history, on the transmission rates of pathogens. Failure to recognize and incorporate the potential effects of host traits into epidemiological models could result in biased estimates of disease transmission dynamics. Therefore, the four chapters included in this thesis focus on exploring the effects of host trait heterogeneity on host- vector interactions at both inter- and intra-specific levels.
Although some vector-borne pathogens (VBPs) cause human diseases, most of them are zoonotic with wildlife serving as their primary vertebrate hosts. Mosquitoes are primary vectors of many VBPs, such as avian Plasmodium and West Nile virus (WNV). Given the important role of mosquitoes and wildlife hosts in the transmission cycle of VBPs, this thesis mainly used a mosquito-borne pathogen, i.e. avian Plasmodium, as the study system, including some of their natural vectors Culex pipiens and Culex restuans and vertebrate hosts, i.e. the House Sparrow (Passer domesticus). Host traits may have profound influence on avian host-mosquito vector interaction, as host-seeking mosquitoes may rely on some host traits to locate potential hosts, resulting in mosquito feeding preferences that produce heterogeneous host-vector contact rates.
Host-seeking activity of mosquitoes is an integrative process that involves multiple senses to detect potential hosts. In this thesis, I first reviewed the role of host morphological, behavioral and physiological traits in mosquito attraction. Mosquito host selection is the outcome of the interaction between innate host preference and extrinsic factors including host attractiveness and availability. Mosquito feeding preference can be readily affected by different host traits producing variations in olfactory, visual, thermal and other cues used in the host-seeking process. I identified knowledge gaps on the role of different host traits in mosquito feeding preference, and highlighted the need of both theoretical and empirical studies on such topic.
To identify the effect of host morphological and behavioral traits on mosquito feeding preference, I conducted a comparative study by combining data of mosquito forage ratios in an avian community from North America with data of avian morphology and behavior. Birds with lighter colors, bigger body size and solitary roosting behavior were bitten more often than expected from their relative abundance in the community. This study highlights the role of host morphological and behavioral traits in interspecific differences in host use patterns of mosquitoes. Future surveillance program for VBPs could consider the larger species roosting alone and/or of lighter colors as good candidates as focal species.
To figure out the role of host physiological traits in mosquito blood-feeding preference, I performed dual-choice experiments by exposing House Sparrows with different metabolic rates to blood-seeking Cx. pipiens and analyzed the relationship between mosquito feeding preference and host metabolism. Individual birds with lower resting metabolic rates were bitten more often than their conspecific counterparts by mosquitoes. This represents the first experimental evidence of a link between host metabolism and vector feeding preference. In addition, birds with greater body mass were bitten more frequently by mosquitoes. As Cx. pipiens is a key vector for multiple VBPs, identifying traits affecting the feeding preference of this mosquito species may throw some light on the epidemiology of these pathogens.
To assess the impact of host infection on blood feeding patterns of mosquitoes, I carried out two dual-choice experiments by exposing House Sparrows with different infection status (i.e. Plasmodium-infected vs. uninfected) and with different infection intensity (manipulated through a medication treatment to reduce the parasite load, i.e. higher Plasmodium load vs. lower – treated- Plasmodium load) to blood-seeking mosquitoes respectively. Individual birds infected with Plasmodium were bitten more often than those infected but treated counterparts. However, the infection status of birds did not significantly affect mosquito feeding pattern, with Plasmodium-infected and uninfected birds bitten similarly by mosquitoes. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behavior in more intensively infected birds, and highlights the importance of considering parasite load in studies on host-vector-pathogen interactions.
By using interdisciplinary approaches that combine comparative methods, molecular analyses as well as empirical bioassays, this thesis identifies several key links between host traits and mosquito feeding preferences at both inter- and intra- specific levels, which may help to better understand the dynamics of host-vector contact rates and hence, the transmission dynamics of VBPs. Incorporating heterogeneity from host traits in future studies may improve our understanding on the ecology of VBDs as well as the surveillance and control efforts in the complex transmission network of VBDs.
Yan, J., Gangoso, L., Martínez-de la Puente, J., Soriguer, R., Figuerola, J. 2017. Avian phenotypic traits related to feeding preferences in two Culex mosquitoes. The Science of Nature, 104:76. doi: 10.1007/s00114-017-1497-x
Yan, J., Martínez-de la Puente, J., Gangoso, L., Gutiérrez-López, R., Soriguer, R., Figuerola, J. 2017. Avian malaria infection intensity influences mosquito feeding patterns. International Journal for Parasitology. doi:10.1016/j.ijpara.2017.09.005