Signs of a vector's adaptive choice: on the evasion of infectious hosts and parasite‐induced mortality

Abstract

Laboratory and field experiments have demonstrated in many cases that malaria vectors do not feed randomly, but show important preferences either for infected or non‐infected hosts. These preferences are likely in part shaped by the costs imposed by the parasites on both their vertebrate and dipteran hosts. However, the effect of changes in vector behaviour on actual parasite transmission remains a debated issue. We used the natural associations between a malaria‐like parasite Polychromophilus murinus, the bat fly Nycteribia kolenatii and a vertebrate host the Daubenton's bat Myotis daubentonii to test the vector's feeding preference based on the host's infection status using two different approaches: 1) controlled behavioural assays in the laboratory where bat flies could choose between a pair of hosts; 2) natural bat fly abundance data from wild‐caught bats, serving as an approximation of realised feeding preference of the bat flies. Hosts with the fewest infectious stages of the parasite were most attractive to the bat flies that did switch in the behavioural assay. In line with the hypothesis of costs imposed by parasites on their vectors, bat flies carrying parasites had higher mortality. However, in wild populations, bat flies were found feeding more based on the bat's body condition, rather than its infection level. Though the absolute frequency of host switches performed by the bat flies during the assays was low, in the context of potential parasite transmission they were extremely high. The decreased survival of infected bat flies suggests that the preference for less infected hosts is an adaptive trait. Nonetheless, other ecological processes ultimately determine the vector's biting rate and thus transmission. Inherent vector preferences therefore play only a marginal role in parasite transmission in the field. The ecological processes rather than preferences per se need to be identified for successful epidemiological predictions.

How a haemosporidian parasite of bats gets around: the genetic structure of a parasite, vector and host compared

“…Although bat fly sampling was not exhaustive in this study, and geography might be a confounding factor, seasonal bottlenecks have been observed in N. schmidlii (Estrada‐Peña & Serra‐Cobo ) as well as other temperate Nycteribia species (Witsenburg et al . ). These severe bottlenecks should decrease the effective population size N e and thereby increase relative levels of differentiation between bat fly populations.…”

“…Although we did not measure the infection status of N. schmidlii here, the infection rate of its sister species Nycteribia kolenatii with the Polychromophilus murinus parasite was 17%, four times lower than of its host M. daubentonii (Witsenburg et al . ). If similar rates were to apply to this system, the effective number of parasite dispersal events caused by vector or host might approach each other.…”

“…On the other hand, this behaviour should cause the females to change hosts more often, increasing their dispersal likelihood. Sex differences in survival have not been observed in bat flies (Marshall 1970;Witsenburg et al 2014). However, the performed experiments concerned short term off-host survival, yet these flies can live up to 6 months at least (Ryberg 1947cited in Marshall 1970; sex differences in long-term survival might therefore very well be possible and have been observed with regard to haemosporidian infections in hippoboscid flies (Waite et al 2012).…”

“…Dispersal rate heterogeneity within species, where infected individuals of a species show different dispersal behaviours compared to their uninfected counterparts, could have caused the discrepancy between host and parasite gene flow. However, N. kolenatii bat flies carrying P. murinus have lower survival than their uninfected counterparts (Witsenburg et al 2014), which should reduce dispersal of infected flies, increasing the parasite population differentiation. No clear effects of a Polychromophilus infection on its bat host have been found as of yet, but an increase in migration behaviour of infected bats, for example being expelled from the current colony as a form of infection avoidance, could cause the parasite to be a more effective disperser than its host population (Curtis 2014).…”

Epidemiological traits of the malaria-like parasite Polychromophilus murinus in the Daubenton¿s bat Myotis daubentonii

“…Heavier adults might be trading off mass against immunity, though it is unclear why this would only affect adults [26]. Like other bat ectoparasites [29], the vector N. kolenatii is attracted to hosts in higher body condition [30]; these bats might therefore be more often exposed to new infections, which causes a slight increase in parasitemia. It might also be a sampling artefact: perhaps for bats with similar levels of infection, only those in good condition can tolerate it enough to go foraging at night when we caught them.…”