Host stress hormones alter vector feeding preferences, success, and productivity

Abstract

Stress hormones might represent a key link between individual-level infection outcome, population-level parasite transmission, and zoonotic disease risk. Although the effects of stress on immunity are well known, stress hormones could also affect host-vector interactions via modification of host behaviours or vector-feeding patterns and subsequent reproductive success. Here, we experimentally manipulated songbird stress hormones and examined subsequent feeding preferences, feeding success, and productivity of mosquito vectors in addition to defensive behaviours of hosts. Despite being more defensive, birds with elevated stress hormone concentrations were approximately twice as likely to be fed on by mosquitoes compared to control birds. Moreover, stress hormones altered the relationship between the timing of laying and clutch size in blood-fed mosquitoes. Our results suggest that host stress could affect the transmission dynamics of vector-borne parasites via multiple pathways.

Extreme Competence: Keystone Hosts of Infections

“…Superattractors and superreceivers are often cast as variants of superspreaders, but their functional roles will depend on covariation between traits affecting (at least) suitability and transmission. In one series of experiments, physiologically stressed, West Nile virus-infected zebra finches (Taeniopygia guttata) attracted twice as many vectors as controls and were infectious to vectors, whereas controls were not [18,19]. There, superattractors were also superspreaders, but in other species low WNV suitability coupled with high vector attractiveness could produce superdiluters.…”

“…One of the best known involves responses to stressors [48]. Variation in stress responses affect multiple aspects of competence in most taxa, but few studies have yet considered whether EC can arise via stress [18,19,49]. Symbionts that live on and within hosts might also affect EC [50], as these organisms sculpt host immune functions and behavior [51,52].…”

Stress hormones predict a host superspreader phenotype in the West Nile virus system

“…Levels of CORT, the main avian glucocorticoid, were altered via implantation of either empty or one or two CORT-filled silastic tubes (Sigma Aldrich, St Louis, MO, product 27840; 7 mm long; inner diameter 1.5 mm, Dow Corning, Midland MI, product 508-006) according to Ouyang et al [29] and identically to Gervasi et al [17]. Birds receiving either one or two implants are hereafter referred to as belonging to 'CORTþ' and 'CORTþþ' treatments (n ¼ 10 in each treatment group); we used two CORT treatments in an attempt to simulate the complex effects of CORT on host immune defences and behaviours [17]. We quantified CORT concentrations in finches 3 days after implant surgery and on the same day as, and immediately prior to, viral inoculations.…”

“…Sensitivity for the assay was approximately 114 pg ml 21 . For more information about experimental hormone manipulation and validation, see electronic supplementary material, Supplementary Methods, figure S1 (see also [17]).…”

“…CORT therefore is apt to affect both intra-and interspecific interactions, which could be important in multi-host pathogen systems. Recently, we reported that a common mosquito vector of West Nile virus, Culex quinquefasciatus, preferentially feeds on songbirds with high CORT despite their higher defensive behaviours (in birds with elevated CORT, relative to controls) towards mosquitoes [17]. Specific mechanisms driving this vector preference are currently unknown, but could be related to metabolic changes associated with elevated CORT, including elevated CO 2 output, host body temperature, or altered host volatile profiles [18].…”