Fitness characteristics of the malaria vector Anopheles funestus during an attempted laboratory colonization

Abstract

Background The malaria vector Anopheles funestus is increasingly recognized as a dominant vector of residual transmission in many African settings. Efforts to better understand its biology and control are significantly impeded by the difficulties of colonizing it under laboratory conditions. To identify key bottlenecks in colonization, this study compared the development and fitness characteristics of wild An. funestus from Tanzania (FUTAZ) and their F1 offspring during colonization attempts. The demography and reproductive success of wild FUTAZ offspring were compared to that of individuals from one of the only An. funestus strains that has been successfully colonized (FUMOZ, from Mozambique) under similar laboratory conditions. Methods Wild An. funestus (FUTAZ) were collected from three Tanzanian villages and maintained inside an insectary at 70–85% RH, 25–27 °C and 12 h:12 h photoperiod. Eggs from these females were used to establish three replicate F1 laboratory generations. Larval development, survival, fecundity, mating success, percentage pupation and wing length were measured in the F1 -FUTAZ offspring and compared with wild FUTAZ and FUMOZ mosquitoes. Results Wild FUTAZ laid fewer eggs (64.1; 95% CI [63.2, 65.0]) than FUMOZ females (76.1; 95% CI [73.3, 79.1]). Survival of F1-FUTAZ larvae under laboratory conditions was low, with an egg-to-pupae conversion rate of only 5.9% compared to 27.4% in FUMOZ. The median lifespan of F1-FUTAZ females (32 days) and males (33 days) was lower than FUMOZ (52 and 49 for females and males respectively). The proportion of female F1-FUTAZ inseminated under laboratory conditions (9%) was considerably lower than either FUMOZ (72%) or wild-caught FUTAZ females (92%). This resulted in nearly zero viable F2-FUTAZ eggs produced. Wild FUTAZ wings appear to be larger compared to the lab reared F1-FUTAZ and FUMOZ. Conclusions This study indicates that poor larval survival, mating success, low fecundity and shorter survival under laboratory conditions all contribute to difficulties in colonizing of An. funestus. Future studies should focus on enhancing these aspects of An. funestus fitness in the laboratory, with the biggest barrier likely to be poor mating.

Wild Populations of Malaria Vectors Can Mate Both Inside and Outside Human Dwellings

“…funestus in laboratories is responsible for the more limited understanding of the biology of this species compared to other vector species. Recent evidence from attempted colonization in Tanzania has highlighted mating as one of the bottlenecks to colonization [45]. The ndings in this current study may therefore enable advancement towards alternative colonization processes either inside laboratories or by using semi-eld chambers and experimental huts in which natural mating can happen.…”

“…To our knowledge, only two strains have been successfully colonized from wild populations despite several attempts, both at the Vector Control Reference Laboratory (VCRL) in the National Institute for Communicable Diseases, South Africa, from populations in Angola (FANG) and Mozambique (FUMOZ) [44]. The FUMOZ strain also maintained at other laboratories worldwide including in Cameroon, UK [75] and Tanzania [45].…”

“…funestus, which dominates malaria transmission in several east and southern Africa zones [3,[40][41][42][43], yet there have been only two successful laboratory colonies using eld-collected material from Mozambique and Angola [44]. Recent evidence from attempted colonization has highlighted mating as one of the bottlenecks to colonization [45]. Studying the conditions of successful mating both outdoors in the wild and in captivity could improve rearing of these and other eurygamic mosquito species.…”

Persistently high proportions of Plasmodium-infected Anopheles funestus mosquitoes in two villages in the Kilombero valley, south-eastern Tanzania

“…Recent studies in Ulanga and Kilombero districts, have demonstrated that Anopheles funestus alone now contributes nearly nine in every ten new infections, even in villages where it is outnumbered by Anopheles arabiensis [6,23]. The species is also strongly resistant to pyrethroids used in the ITNs [24], survives much longer than its counterparts [6,25] and is strongly adapted to primarily bite humans over other vertebrates [26]. While no detailed analysis has been conducted, it is hypothesized that villages currently having the greatest malaria prevalence are those with highest densities of An.…”

CRISPR-mediated knock-in of transgenes into the malaria vectorAnopheles funestus

“…funestus still remains the exception. This may in part simply reflect the logistical difficulty associated with rearing this species in the laboratory (Hunt et al 2005;Ngowo et al 2021;Morgan et al 2010), but may also reflect a quirk in its biology that make it more refractory to the process of germline transformation.…”