Limits...
Leishmania manipulation of sand fly feeding behavior results in enhanced transmission.

Rogers ME, Bates PA - PLoS Pathog. (2007)

Bottom Line: A key feature of parasite development in the sand fly gut is the secretion of a gel-like plug composed of filamentous proteophosphoglycan.Further, Leishmania infection specifically causes an increase in vector biting persistence on mice (re-feeding after interruption) and also promotes feeding on multiple hosts.Thus, we demonstrate that behavioral manipulation of the infected vector provides a selective advantage to the parasite by significantly increasing transmission.

View Article: PubMed Central - PubMed

Affiliation: Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

ABSTRACT
In nature the prevalence of Leishmania infection in whole sand fly populations can be very low (<0.1%), even in areas of endemicity and high transmission. It has long since been assumed that the protozoan parasite Leishmania can manipulate the feeding behavior of its sand fly vector, thus enhancing transmission efficiency, but neither the way in which it does so nor the mechanisms behind such manipulation have been described. A key feature of parasite development in the sand fly gut is the secretion of a gel-like plug composed of filamentous proteophosphoglycan. Using both experimental and natural parasite-sand fly combinations we show that secretion of this gel is accompanied by differentiation of mammal-infective transmission stages. Further, Leishmania infection specifically causes an increase in vector biting persistence on mice (re-feeding after interruption) and also promotes feeding on multiple hosts. Both of these aspects of vector behavior were found to be finely tuned to the differentiation of parasite transmission stages in the sand fly gut. By experimentally accelerating the development rate of the parasites, we showed that Leishmania can optimize its transmission by inducing increased biting persistence only when infective stages are present. This crucial adaptive manipulation resulted in enhanced infection of experimental hosts. Thus, we demonstrate that behavioral manipulation of the infected vector provides a selective advantage to the parasite by significantly increasing transmission.

Show MeSH

Related in: MedlinePlus

Feeding Persistence and Transmission of Leishmania to Multiple HostsFlies were fed blood alone (open square), L. infantum (dotted square), L. mexicana stationary phase (shaded square), or exponential phase amastigotes (closed square). The number of flies feeding on a different host when interrupted was determined on days 5, 7, and 10 post-infection/feeding in a behavioral assay. n = 12 per point, representing the combination of two independent experiments. Error bars 1 s.e.m. Asterisks indicate values that are statistically significant (*p < 0.05, **p < 0.005) from blood fed control flies using an unpaired t-test.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC1904410&req=5

ppat-0030091-g004: Feeding Persistence and Transmission of Leishmania to Multiple HostsFlies were fed blood alone (open square), L. infantum (dotted square), L. mexicana stationary phase (shaded square), or exponential phase amastigotes (closed square). The number of flies feeding on a different host when interrupted was determined on days 5, 7, and 10 post-infection/feeding in a behavioral assay. n = 12 per point, representing the combination of two independent experiments. Error bars 1 s.e.m. Asterisks indicate values that are statistically significant (*p < 0.05, **p < 0.005) from blood fed control flies using an unpaired t-test.

Mentions: Importantly, for the increase in feeding persistence of infected flies to be of adaptive value to the parasite the behavior must lead to increased transmission. During a transmission attempt interruption to blood feeding can arise either from an insufficient blood flow to the bite site or from the activation of host defensive behavior [2,23]. In both scenarios a partial blood meal is likely to promote a fly to re-feed in order to obtain sufficient nutrients for egg-maturation, and as indicated above, persistence is further enhanced in the case of a Leishmania-infected sand fly. Although re-feeding on the same host would clearly benefit the parasite, re-feeding on multiple hosts is particularly advantageous as this will increase the basic reproduction number (R0) of the infection (the number of new cases of a disease that arises from a single infection). Such behavior has been proposed with malaria-infected mosquitoes [24], but there is only circumstantial evidence for this to apply to Leishmania-infected sand flies [25,26]. Therefore, we modified the interruption-behavioral assay by including a second anaesthetized mouse in the cage to assess the probability of the fly choosing to feed on a different host when interrupted (Figure 4). Flies were tested at 5, 7, and 10 d post-infection to provide infections at different stages of metacyclogenesis (beginning, middle, and end) for both Leishmania species. The results showed that infection with both L. infantum and L. mexicana promoted feeding on multiple hosts, whereas uninfected flies in most cases gave up completely when interrupted. Furthermore, this behavior correlated with metacyclogenesis, because exponential phase L. mexicana infections exhibited an increased and earlier tendency to initiate a feed on a new host earlier than infections initiated with stationary phase L. mexicana amastigotes (p < 0.005). These data demonstrated that persistent feeding behavior can lead to an increase in the number of hosts that become infected.


Leishmania manipulation of sand fly feeding behavior results in enhanced transmission.

Rogers ME, Bates PA - PLoS Pathog. (2007)

Feeding Persistence and Transmission of Leishmania to Multiple HostsFlies were fed blood alone (open square), L. infantum (dotted square), L. mexicana stationary phase (shaded square), or exponential phase amastigotes (closed square). The number of flies feeding on a different host when interrupted was determined on days 5, 7, and 10 post-infection/feeding in a behavioral assay. n = 12 per point, representing the combination of two independent experiments. Error bars 1 s.e.m. Asterisks indicate values that are statistically significant (*p < 0.05, **p < 0.005) from blood fed control flies using an unpaired t-test.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1904410&req=5

ppat-0030091-g004: Feeding Persistence and Transmission of Leishmania to Multiple HostsFlies were fed blood alone (open square), L. infantum (dotted square), L. mexicana stationary phase (shaded square), or exponential phase amastigotes (closed square). The number of flies feeding on a different host when interrupted was determined on days 5, 7, and 10 post-infection/feeding in a behavioral assay. n = 12 per point, representing the combination of two independent experiments. Error bars 1 s.e.m. Asterisks indicate values that are statistically significant (*p < 0.05, **p < 0.005) from blood fed control flies using an unpaired t-test.
Mentions: Importantly, for the increase in feeding persistence of infected flies to be of adaptive value to the parasite the behavior must lead to increased transmission. During a transmission attempt interruption to blood feeding can arise either from an insufficient blood flow to the bite site or from the activation of host defensive behavior [2,23]. In both scenarios a partial blood meal is likely to promote a fly to re-feed in order to obtain sufficient nutrients for egg-maturation, and as indicated above, persistence is further enhanced in the case of a Leishmania-infected sand fly. Although re-feeding on the same host would clearly benefit the parasite, re-feeding on multiple hosts is particularly advantageous as this will increase the basic reproduction number (R0) of the infection (the number of new cases of a disease that arises from a single infection). Such behavior has been proposed with malaria-infected mosquitoes [24], but there is only circumstantial evidence for this to apply to Leishmania-infected sand flies [25,26]. Therefore, we modified the interruption-behavioral assay by including a second anaesthetized mouse in the cage to assess the probability of the fly choosing to feed on a different host when interrupted (Figure 4). Flies were tested at 5, 7, and 10 d post-infection to provide infections at different stages of metacyclogenesis (beginning, middle, and end) for both Leishmania species. The results showed that infection with both L. infantum and L. mexicana promoted feeding on multiple hosts, whereas uninfected flies in most cases gave up completely when interrupted. Furthermore, this behavior correlated with metacyclogenesis, because exponential phase L. mexicana infections exhibited an increased and earlier tendency to initiate a feed on a new host earlier than infections initiated with stationary phase L. mexicana amastigotes (p < 0.005). These data demonstrated that persistent feeding behavior can lead to an increase in the number of hosts that become infected.

Bottom Line: A key feature of parasite development in the sand fly gut is the secretion of a gel-like plug composed of filamentous proteophosphoglycan.Further, Leishmania infection specifically causes an increase in vector biting persistence on mice (re-feeding after interruption) and also promotes feeding on multiple hosts.Thus, we demonstrate that behavioral manipulation of the infected vector provides a selective advantage to the parasite by significantly increasing transmission.

View Article: PubMed Central - PubMed

Affiliation: Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

ABSTRACT
In nature the prevalence of Leishmania infection in whole sand fly populations can be very low (<0.1%), even in areas of endemicity and high transmission. It has long since been assumed that the protozoan parasite Leishmania can manipulate the feeding behavior of its sand fly vector, thus enhancing transmission efficiency, but neither the way in which it does so nor the mechanisms behind such manipulation have been described. A key feature of parasite development in the sand fly gut is the secretion of a gel-like plug composed of filamentous proteophosphoglycan. Using both experimental and natural parasite-sand fly combinations we show that secretion of this gel is accompanied by differentiation of mammal-infective transmission stages. Further, Leishmania infection specifically causes an increase in vector biting persistence on mice (re-feeding after interruption) and also promotes feeding on multiple hosts. Both of these aspects of vector behavior were found to be finely tuned to the differentiation of parasite transmission stages in the sand fly gut. By experimentally accelerating the development rate of the parasites, we showed that Leishmania can optimize its transmission by inducing increased biting persistence only when infective stages are present. This crucial adaptive manipulation resulted in enhanced infection of experimental hosts. Thus, we demonstrate that behavioral manipulation of the infected vector provides a selective advantage to the parasite by significantly increasing transmission.

Show MeSH
Related in: MedlinePlus