Anopheles is a genus of mosquito (Culicidae). There are approximately 460 recognised species: while over 100 can transmit human malaria, only 30-40 commonly transmit parasites of the genus Plasmodium that cause malaria which affects humans in endemic areas. Anopheles gambiae is one of the best known, because of its predominant role in the transmission of the deadly species - Plasmodium falciparum.
The Culicine and Anopheles clades diverged ~150 million years ago.[1] The Old and New World Anopheles species subsequently diverged ~95 million years ago.[1]
Systematics
The genus Anopheles belongs to a subfamily Anophelinae with three genera: Anopheles Meigen (nearly worldwide distribution), Bironella Theobald (Australia only) and Chagasia Cruz (Neotropics). Bironella appears to be the sister taxon to the Anopheles with Chagasia forming the outgroup in this subfamily.
The classification of this genus began in 1901 with Theobald. Despite the passage of time the taxonomy remains incompletely settled. Classification into species is based on morphological characteristics - wing spots, head anatomy, larval and pupal anatomy, chromosome structure - and more recently on DNA sequences.
The genus itself has been subdivided into seven subgenera based primarily on the number and positions of specialized setae on the gonocoxites of the malegenitalia. The system of subgenera originated with the work of Christophers who in 1915 described three subgenera: Anopheles (widely distributed), Myzomyia (later renamed Cellia) (Old World) and Nyssorhynchus (Neotropical). Nyssorhynchus was first described as Lavernia by Theobald. Edwards in 1932 added the subgenus Stethomyia (Neotropical distribution). Kerteszia was also described by Edwards in 1932 but then recognised as a subgrouping of Nyssorhynchus. It was elevated to subgenus status by Komp in 1937 and it is also found in the Neotropics. Two additional subgenera have since been recognised: Baimaia (Southeast Asia only) by Harbach et al in 2005 and Lophopodomyia (Neotropical) by Antunes in 1937.
Within the genus Anopheles there are two main groupings: one formed by the Cellia and Anopheles subgenera and a second by Kerteszia, Lophopodomyia and Nyssorhynchus. Subgenus Stethomyia is an outlier with respect to these two taxa. Within the second group Kerteszia and Nyssorhynchus appear to be sister taxa.
The number of species currently recognised within the subgenera is given here in parentheses: Anopheles (206 species), Baimaia (1), Cellia (216), Kerteszia (12), Lophopodomyia (6), Nyssorhynchus (34) and Stethomyia (5).
Taxonomic units between subgenus and species are not currently recognised as official zoological names. In practice a number of taxonomic levels have been introduced. The larger subgenera (Anopheles, Cellia and Nyssorhynchus) have been subdivided into sections and series which in turn have been divided into groups and subgroups. Below subgroup but above species level is the species complex. Taxonomic levels above species complex can be distinguished on morphological grounds. Species within a species complex are either morphologically identical or extremely similar and can only be reliably separated by microscopic examination of the chromosomes or DNA sequencing. The classification continues to be revised.
Subgenus Nyssorhynchus has been divided in three sections: Albimanus (19 species), Argyritarsis (11 species) and Myzorhynchella (4 species). The Argyritarsis section has been sub divided into Albitarsis and Argyritarsis groups.
The Anopheles Group was divided by Edwards into four series: Anopheles (worldwide), Myzorhynchus (Palearctic, Oriental, Australasian and Afrotropical), Cycloleppteron (Neotropical) and Lophoscelomyia (Oriental); and two groups, Arribalzagia (Neotropical) and Christya (Afrotropical). Reid and Knight (1961) modified this classification and consequently subdivided the subgenus Anopheles into two sections, Angusticorn and Laticorn and six series. The Arribalzagia and Christya Groups were considered to be series. The Laticorn Section includes the Arribalzagia (24 species), Christya and Myzorhynchus Series. The Angusticorn Section includes members of the Anopheles, Cycloleppteron and Lophoscelomyia Series.
Anopheles bonneorum Fonseca & Ramos is considered to be a synonym of Anopheles costai.
Life stages
Like all mosquitoes, anophelines go through four stages in their life cycle: egg, larva, pupa, and imago. The first three stages are aquatic and last 5-14 days, depending on the species and the ambient temperature. The adult stage is when the female Anopheles mosquito acts as malariavector. The adult females can live up to a month (or more in captivity) but most probably do not live more than 1-2 weeks in nature.
Eggs
Adult females lay 50-200 eggs per oviposition. Eggs are laid singly directly on water and are unique in having floats on either side. Eggs are not resistant to drying and hatch within 2-3 days, although hatching may take up to 2-3 weeks in colder climates.
Larvae
Anopheles larva from southern Germany, about 8 mm long.
Mosquito larvae have a well-developed head with mouth brushes used for feeding, a large thorax and a segmented abdomen. They don't have legs. In contrast to other mosquitoes, Anopheles larvae lack a respiratory siphon and for this reason position themselves so that their body is parallel to the surface of the water.
Larvae breathe through spiracles located on the 8th abdominal segment and therefore must come to the surface frequently. The larvae spend most of their time feeding on algae, bacteria, and other microorganisms in the surface microlayer. They dive below the surface only when disturbed. Larvae swim either by jerky movements of the entire body or through propulsion with the mouth brushes.
Larvae develop through 4 stages, or instars, after which they metamorphose into pupae. At the end of each instar, the larvae molt, shedding their exoskeleton, or skin, to allow for further growth.
The larvae occur in a wide range of habitats but most species prefer clean, unpolluted water. Larvae of Anopheles mosquitoes have been found in fresh- or salt-water marshes, mangrove swamps, rice fields, grassy ditches, the edges of streams and rivers, and small, temporary rain pools. Many species prefer habitats with vegetation. Others prefer habitats that have none. Some breed in open, sun-lit pools while others are found only in shaded breeding sites in forests. A few species breed in tree holes or the leaf axils of some plants.
Pupae
The pupa is comma-shaped when viewed from the side. The head and thorax are merged into a cephalothorax with the abdomen curving around underneath. As with the larvae, pupae must come to the surface frequently to breathe, which they do through a pair of respiratory trumpets on the cephalothorax. After a few days as a pupa, the dorsal surface of the cephalothorax splits and the adult mosquito emerges.
Adults
The duration from egg to adult varies considerably among species and is strongly influenced by ambient temperature. Mosquitoes can develop from egg to adult in as little as 5 days but usually take 10-14 days in tropical conditions.
Like all mosquitoes, adult Anopheles have slender bodies with 3 sections: head, thorax and abdomen.
The head is specialized for acquiring sensory information and for feeding. The head contains the eyes and a pair of long, many-segmented antennae. The antennae are important for detecting host odors as well as odors of breeding sites where females lay eggs. The head also has an elongated, forward-projecting proboscis used for feeding, and two sensory palps.
The thorax is specialized for locomotion. Three pairs of legs and a pair of wings are attached to the thorax.
The abdomen is specialized for food digestion and egg development. This segmented body part expands considerably when a female takes a blood meal. The blood is digested over time serving as a source of protein for the production of eggs, which gradually fill the abdomen.
Anopheles mosquitoes can be distinguished from other mosquitoes by the palps, which are as long as the proboscis, and by the presence of discrete blocks of black and white scales on the wings. Adult Anopheles can also be identified by their typical resting position: males and females rest with their abdomens sticking up in the air rather than parallel to the surface on which they are resting.
Adult mosquitoes usually mate within a few days after emerging from the pupal stage. In most species, the males form large swarms, usually around dusk, and the females fly into the swarms to mate.
Males live for about a week, feeding on nectar and other sources of sugar. Females will also feed on sugar sources for energy but usually require a blood meal for the development of eggs. After obtaining a full blood meal, the female will rest for a few days while the blood is digested and eggs are developed. This process depends on the temperature but usually takes 2-3 days in tropical conditions. Once the eggs are fully developed, the female lays them and resumes host seeking.
The cycle repeats itself until the female dies. While females can live longer than a month in captivity, most do not live longer than 1-2 weeks in nature. Their lifespan depends on temperature, humidity, and also their ability to successfully obtain a blood meal while avoiding host defenses.
Habitat
Although malaria is nowadays limited to tropical areas, most notoriously regions of sub-Saharan Africa, many Anopheles species live in colder latitudes (see this map from the CDC). Indeed, malaria outbreaks have, in the past, occurred in colder climates, for example during the construction of the Rideau Canal in Canada during the 1820s. Since then, the Plasmodium parasite (not the Anopheles mosquito) has been eradicated from first world countries.
The CDC warns, however, that "Anopheles that can transmit malaria are found not only in malaria-endemic areas, but also in areas where malaria has been eliminated. The latter areas are thus constantly at risk of re-introduction of the disease."
Susceptibility to become a vector of disease
Some species are poor vectors of malaria, as the parasites do not develop well (or at all) within them. There is also variation within species. In the laboratory, it has been possible to select for strains of A. gambiae that are refractory to infection by malaria parasites. These refractory strains have an immune response that encapsulates and kills the parasites after they have invaded the mosquito's stomach wall. Scientists are studying the genetic mechanism for this response. It is hoped that some day, genetically modified mosquitoes that are refractory to malaria can replace wild mosquitoes, thereby limiting or eliminating malaria transmission.
Malaria transmission and control
Understanding the biology and behavior of Anopheles mosquitoes can help understand how malaria is transmitted and can aid in designing appropriate control strategies. Factors that affect a mosquito's ability to transmit malaria include its innate susceptibility to Plasmodium, its host choice and its longevity. Factors that should be taken into consideration when designing a control program include the susceptibility of malaria vectors to insecticides and the preferred feeding and resting location of adult mosquitoes.
On December 21, 2007, a study published in PLoS Pathogens found that the hemolytic C-type lectin CEL-III from Cucumaria echinata, a sea cucumber found in the Bay of Bengal, impaired the development of the malaria parasite when produced by transgenic A. stephensi.[2] This could potentially be used one day to control malaria by spreading genetically modified mosquitoes refractory to the parasites, although there are numerous scientific and ethical issues to be overcome before such a control strategy could be implemented.
Preferred sources for blood meals
One important behavioral factor is the degree to which an Anopheles species prefers to feed on humans (anthropophily) or animals such as cattle (zoophily). Anthropophilic Anopheles are more likely to transmit the malaria parasites from one person to another. Most Anopheles mosquitoes are not exclusively anthropophilic or zoophilic. However, the primary malaria vectors in Africa, A. gambiae and A. funestus, are strongly anthropophilic and, consequently, are two of the most efficient malaria vectors in the world.
Once ingested by a mosquito, malaria parasites must undergo development within the mosquito before they are infectious to humans. The time required for development in the mosquito (the extrinsic incubation period) ranges from 10-21 days, depending on the parasite species and the temperature. If a mosquito does not survive longer than the extrinsic incubation period, then she will not be able to transmit any malaria parasites.
It is not possible to measure directly the life span of mosquitoes in nature. But indirect estimates of daily survivorship have been made for several Anopheles species. Estimates of daily survivorship of A. gambiae in Tanzania ranged from 0.77 to 0.84 meaning that at the end of one day between 77% and 84% will have survived.[3]
Assuming this survivorship is constant through the adult life of a mosquito, less than 10% of female A. gambiae would survive longer than a 14-day extrinsic incubation period. If daily survivorship increased to 0.9, over 20% of mosquitoes would survive longer than a 14-day extrinsic incubation period. Control measures that rely on insecticides (e.g. indoor residual spraying) may actually impact malaria transmission more through their effect on adult longevity than through their effect on the population of adult mosquitoes.
Patterns of feeding and resting
Most Anophelesmosquitoes are crepuscular (active at dusk or dawn) or nocturnal (active at night). Some Anopheles mosquitoes feed indoors (endophagic) while others feed outdoors (exophagic). After feeding on some blood mosquitoes prefer to rest indoors (endophilic) while others prefer to rest outdoors (exophilic), though this can differ regionally based on local vector ecotype, and vector chromosomal makeup, as well as housing type and local microclimatic conditions. Biting by nocturnal, endophagic Anopheles mosquitoes can be markedly reduced through the use of insecticide-treated bed nets (ITNs) or through improved housing construction to prevent mosquito entry (e.g. window screens). Endophilic mosquitoes are readily controlled by indoor spraying of residual insecticides. In contrast, exophagic/exophilic vectors are best controlled through source reduction (destruction of the breeding sites).
Insecticide resistance
Insecticide-based control measures (e.g. indoor spraying with insecticides, ITNs) are the principal way to kill mosquitoes that bite indoors. However, after prolonged exposure to an insecticide over several generations, mosquitoes, like other insects, may develop resistance, a capacity to survive contact with an insecticide. Since mosquitoes can have many generations per year, high levels of resistance can arise very quickly. Resistance of mosquitoes to some insecticides has been documented with just within a few years after the insecticides were introduced. There are over 125 mosquito species with documented resistance to one or more insecticides. The development of resistance to insecticides used for indoor residual spraying was a major impediment during the Global Malaria Eradication Campaign. Judicious use of insecticides for mosquito control can limit the development and spread of resistance. However, use of insecticides in agriculture has often been implicated as contributing to resistance in mosquito populations. It is possible to detect developing resistance in mosquitoes and control programs are well advised to conduct surveillance for this potential problem.
^ ab Calvo E, Pham VM, Marinotti O, Andersen JF, Ribeiro JM. (2009) The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics. 10(1):57
^(Charlwood et al., 1997, Survival And Infection Probabilities of Anthropophagic Anophelines From An Area of High Prevalence of Plasmodium falciparum in Humans, Bulletin of Entomological Research, 87, 445-453)
Walter Reed Biosystematics Unit. - Links to the online mosquito catalog, keys for mosquito identification, images and information on medically important species and much more.
