Adaptation of a Filarial Worm, Brugia patei, to a New Mosquito Host, Aedes togoi

Abstract

1. The filarial worm Brugia patei was brought to London from East Africa in the larval stage developing in Mansonia mosquitoes. Subsequent transmission to domestic cats was possible in London through a laboratory colony of Mansonia uniformis and the worm was very infective to this species of mosquito. The worm was much less infective to Aedes togoi and Anopheles gambiae.2. Subsequent passage of the worm through Aedes togoi has increased its infectivity to this species of mosquito. The infection rate has risen from 43·6% in females of A. togoi fed on the cat original- ly infected by larvae from Mansonia mosquitoes, to 59·2% in females fed on a cat containing the first generation of worms to pass through A. togoi, to 79·1% in females fed on cats containing the second generation of worms to pass through A. togoi, to 86·7% in females fed on cats containing the third generation of worms to pass through A. togoi, to 89·8% in females fed on cats containing the fourth generation of worms to pass through A. togoi.3. The distributions of infective stage larvae in female mosquitoes were negative binomial distributions. These were related to the distributions of microfilarial intake immediately after infection which were also negative binomial. From one generation of worms passed through the new mosquito host to the next the mean and the k value of the negative binomial of the infective stage larvae approached the same parameters for the distribution of microfilarial intake. By the fourth generation of worms passed through A. togoi the distributions of microfilarial intake and infective stage larvae developing in A. togoi were similar, suggesting close adaptation to the new mosquito host. A similar relation between these distributions was found originally in Mansonia. There were however considerable differences in these distributions between the two species of mosquito.4. The experiment extended over a period of 6 years. The change in infectivity did not appear to be related to the microfilarial density, age of infection, or sex, in the mammalian host. Neither could it be related to the genetics of susceptibility in the mosquito, nor to mosquito culture techniques, nor to mosquito mortality.5. It is concluded that the observed change in infectivity is best explained by a change in adaptation of the worm to the new intermediate host by selection within the mosquito of those microfilariae adapted to it. No major change in infectivity to the original intermediate host, Mansonia, was found during the experiment.6. These findings are examined with reference to changes in adaptation to mosquito hosts in the history of Bancroftian filariasis.

Use of microarray hybridization to identify Brugia genes involved in mosquito infectivity

“…Little attention has been paid to the parasite's role in this complex interaction even though it is equally important in determining infection outcome. This was elegantly demonstrated by the repeated passage of Brugia patei in a partially permissive vector, Aedes togoi, that resulted in increased infectivity over generations (Laurence and Pester 1967). These findings provide clear evidence that the complex interaction of Brugia with its vector undoubtedly is mediated genetically by both the vector and the parasite, and provide a model for successful adaptation of filarial worms to new vector species.…”

Midgut Barrier Imparts Selective Resistance to Filarial Worm Infection in Culex pipiens pipiens

“…For example, in the case of Plasmodium parasites that cause human and avian malaria, destruction of ookinetes by digestive enzymes can occur in the midgut lumen, increased nitric oxide production and superoxide anion production can kill ookinetes, ookinetes can be killed by pattern-recognition receptor mediated phagocytosis [32], the absence of molecular recognition sites on midgut cells can prevent ookinete invasion [33], intracellular Plasmodium ookinetes can be lysed [34], oocysts can be targeted by phagocyte attack, and oocysts can be encapsulated and melanized [32]. Successful pathogen development is clearly dependent on vector cells and molecules, and on the genetic makeup of the pathogen itself, as evidenced by the selection of arboviruses for attenuation in mosquito vectors and vertebrate hosts [31], differential susceptibility of culicine and anopheline mosquitoes to avian and human malaria parasites [34]; and the selection of filarial worms for increased infectivity in a permissive vector [35].…”

Migrations des microfilaires et des peuples océaniens. Une approche de la spéciation chez les filaires de Bancroft et de Malaisie, par l’étude de la périodicité des microfilaires en fonction de la densité ; contribution à la préhistoire du Pacifique

“…Laurence et Pester (1967) l'ont démontré en laboratoire, et citent des exemples convaincants d'adaptation dans les conditions naturelles de filaires à des nouvelles espèces vectrices, en quelques dizaines d'années.…”

“…Tout en conservant sa pério dicité nocturne, elle s'y est adaptée à d 'autres vecteurs, suivant le processus mis en évidence par Laurence et Pester (1967). Cette adaptabilité s'est maintenue, puisque le vecteur principali aux Philippines, après avoir été un Anophèle, est actuellement Aedes (Finlaya) poicilius : ses gîtes larvaires étant constitués par les aisselles de bana niers, il s'est considérablement développé avec les grandes plantations d'abaca (chanvre de Manille) du siècle dernier (Cabrera et Rozeboom, 1965).…”

“…pacifica subpériodique comme provenant de l'adaptation du type général, périodique nocturne, à des moustiques d'agressivité principalement diurne. Cette thèse est défendue, avec différents arguments, par la majorité des auteurs (en particulier Buxton, 1928 ;Mattingly, 1965 ;Iyengar, 1965 ;Rozeboom et Cabrera, 1966 ;Laurence et Pester, 1967 ;Schacher et Geddawi, 1969). En ce qui concerne B. malayi, Wharton (1963) pense également que la forme subpériodique est ultérieure à la forme périodique.…”