Superfamily Culicoidea | Order Diptera Family Culicidae | |
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Anopheles is a genus of mosquitoes (Culicidae). Of about 484 recognised species, over 100 can transmit human malaria, but 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.
Contents
Classification
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, and chromosome structure, and more recently on DNA sequences.
The genus Anopheles belongs to a subfamily Anophelinae with three genera: Anopheles Meigen (nearly worldwide distribution), Bironella Theobald (Australia only: 11 described species) and Chagasia Cruz (Neotropics: four described species). The genus Bironella has been divided into three subgenera: Bironella Theobald (two species), Brugella Edwards (three species) and Neobironella Tenorio (three species). Bironella appears to be the sister taxon to the Anopheles, with Chagasia forming the outgroup in this subfamily.
The type species of the genus is Anopheles maculipennis.
Subgenera
The genus has been subdivided into seven subgenera based primarily on the number and positions of specialized setae on the gonocoxites of the male genitalia. 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 was recognised as a subgrouping of Nyssorhynchus. It was elevated to subgenus status by Komp in 1937; this subgenus 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.
One species within each subgenus has been identified as the type species of that particular subgenus:
Within the genus Anopheles 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. Cellia appears to be more closely related to the Kerteszia-Lophopodomyia-Nyssorhynchus group than to Anopheles or Stethomyia, tentatively suggesting the following branching order: ( Stethomyia ( Anopheles ( Cellia ( Lophopodomyia ( Kerteszia, Nyssorhynchus))))).
The number of species currently recognised within the subgenera is given here in parentheses: Anopheles (206 species), Baimaia (one), Cellia (239), Kerteszia (12), Lophopodomyia (six), Nyssorhynchus (34) and Stethomyia (fuve).
The subgenus Baimaia may be elevated to genus level, as it appears to be a sister group to Bironella and all other Anopheles.
The ancestors of Drosophila and Anopheles diverged 260 million years ago. The Old and New World Anopheles species subsequently diverged between 80 and 95 million years ago.
Divisions below subgenus
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.
The first species complex was described in 1926 when the problem of nontransmission of malaria by Anopheles gambiae was solved by Falleroni, who recognised that An. gambiae was a complex of six species, of which only four could transmit malaria. This complex has subsequently been revised to a total of seven species of which five transmit malaria.
Subgenus Nyssorhynchus has been divided in three sections: Albimanus (19 species), Argyritarsis (11 species) and Myzorhynchella (four species). The Argyritarsis section has been subdivided 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 by subdividing the subgenus Anopheles into two sections, Angusticorn and Laticorn and six series. The division was based on the shape of their pupal trumpets. The Laticorn section was created for those species with wide, funnel-shaped trumpets having the longest axis transverse to the stem, and the Angusticorn section for species with semitubular trumpets having the longest axis vertical more or less in line with the stem. The earlier Arribalzagia and Christya groups were considered to be series. The Angusticorn section includes members of the Anopheles, Cycloleppteron, and Lophoscelomyia series, and the Laticorn section includes the Arribalzagia (24 species), Christya, and Myzorhynchus series.
Cellia is the largest subgenus: all species within this subgenus are found in the Old World. It has been divided into six series - Cellia (eight species), Myzomyia (69 species), Neocellia (33 species), Neomyzomyia (99 species), Paramyzomyia (six species) and Pyretophorus (22 species). This classification was developed by Grjebine (in 1966), Reid (in 1968), and Gillies & de Meillon (also in 1968) based on the work by Edwards in 1932. Series definition within this subgenus is based on the cibarial armature - a collection of specialized spicules borne ventrally at the posterior margin of the cibarium - which was first used as a taxonomic method by Christophers in 1933.
Kerteszia is a small subgenus found in South America whose larvae have specific ecological requirements; these can only develop within water that accumulates at the base of the follicular axis of the epiphytic Bromeliaceae. Unlike the majority of mosquitoes, species in this subgenus are active during the day.
Within a number of species, separate subspecies have been identified. The diagnostic criteria and characteristic features of each subgenus are discussed on the own page.
Species complexes
Anopheles nuneztovari is a species complex with at least one occurring in Colombia and Venezuela and another occurring in the Amazon Basin. These clades appear to have diverged and expanded in the Pleistocene.
Medical and veterinary importance
The first demonstration that mosquitoes could act as vectors of disease was by Patrick Manson, a British physician working in China, who showed that a Culex species could transmit filariasis in 1878. This was then followed in 1897 by Ronald Ross, who showed avian malaria could also be transmitted by a species of Culex. Grassi in Italy showed that the species causing human malaria were transmitted by species of the genus Anopheles in 1898. Anopheles gambiae (then Anopheles coastalis), the most important of the vectors transmitting human malaria, was first recognised as such in 1899 at Freetown, Sierra Leone. It was later realised that only a small number of species of mosquitoes were responsible for the vast majority of human malaria and other diseases. This generated a considerable interest in the taxonomy of this and other mosquito genera.
The species of the subgenera Baimaia, Lophopodomyia, and Stethomyia are not of medical importance.
All species within the subgenus Anopheles known to carry human malaria lie within either the Myzorhynchus or the Anopheles series. Anopheles maculipennis s.l. is a known vector of West Nile virus.
Six species in the subgenus Kerteszia can carry human malaria. Of these, only An. bellator and An. cruzii are of importance. Anopheles bellator can also transmit Wuchereria bancrofti.
Several species of the subgenus Nyssorhynchus are of medical importance.
All series of the subgenus Cellia contain vectors of malarial protozoa and microfilariae.
Five species of anopheline mosquitoes (An. arabiensis, An. funestus, An. gambiae, An. moucheti, An. nili) all belonging to the subgenus Cellia are responsible for over 95% of total malaria transmission for Plasmodium falciparum in continental sub-Saharan Africa.
Anopheles sundaicus and An. subpictus are important vectors of Plasmodium vivax.
Species evolution
The Anopheles gambiae complex has a number of important malaria vectors. A chromosomal study suggests that An. merus is the basal member of this complex and is sister species to An. gambiae. The two species An. quadriannulatus A and An. quadriannulatus B - neither of whom are vectors for malaria - are derived from An. gambiae.
The subgenera Anopheles and Cellia appear to be sister clades as do Kerteszia and Nyssorhynchus.
Species listing
Species that have been shown to be vectors of human malaria are marked with a star (*) after the name.
Subgenus Anopheles
Anopheles anthropophagus* Xu & Feng 1975Anopheles confusaAnopheles derooki Soesilo & Van Slooten 1931Anopheles gracilis Theobald 1905Anopheles hollandi Taylor 1934Anopheles obscura Tenorio 1975Anopheles papuae Swellengrebel & Swellengrebel de Graaf 1919Anopheles simmondsi Tenorio 1977Anopheles travestita Brug 1928Section AngusticornSection Laticorn (Reid & Knight 1961)Subgenus Baimaia
Anopheles kyondawensisAbraham 1947Subgenus Cellia
Anopheles rageaui Mattingly and Adam
Series Cellia (Christophers 1924)
Anopheles argenteolobatus Gough 1910Anopheles brumpti Hamon & Rickenbach 1955Anopheles carnevalei Brunhes le Goff & Geoffroy 1999Anopheles cristipalpis Service 1977Anopheles murphyi Gillies 1968Anopheles pharoensis Theobald 1901Anopheles swahilicus Gillies 1964Group Squamosus (Grjebine 1966)Anopheles cydippis de Meillon 1931Anopheles squamosusTheobald 1901Series Myzomyia
Anopheles apoci Marsh 1933Anopheles azaniae Bailly-Choumara 1960Anopheles barberellus Evans 1932Anopheles brunnipes Theobald 1910Anopheles domicola Edwards 1916Anopheles dthali Patton 1905Anopheles erythraeus Corradetti 1939Anopheles ethiopicus Gillies & Coetzee 1987Anopheles flavicosta Edwards 1911Anopheles fontinalis Gillies 1968Anopheles majidi Young & Majid 1928Anopheles moucheti* Evans 1925subspecies bervoetsi D'Haenans 1961subspecies moucheti Evans 1925subspecies nigeriensisAnopheles schwetzi Evans 1934Anopheles tchekedii de Meillon & Leeson 1940Anopheles walravensi Edwards 1930Group Demeilloni (Gillies & De Meillon 1962)Anopheles carteri Evans & de Meillon 1933Anopheles demeilloni Evans 1933Anopheles freetownensis Evans 1925Anopheles garnhami Edwards 1930Anopheles keniensis Evans 1931Anopheles lloreti Gil Collado 1936Anopheles sergentii* Theobald 1907subspecies macmahoni Evans 1936subspecies sergentii Theobald 1907Group Funestus (Garros et al 2004)Anopheles jeyporiensis James 1902Group MarshalliiAnopheles austenii Theobald 1905Anopheles berghei Vincke & Leleup 1949Anopheles brohieri Edwards 1929Anopheles gibbinsi Evans 1935Anopheles hancocki Edwards 1929Anopheles hargreavesi Evans 1927Anopheles harperi Evans 1936Anopheles mortiauxi Edwards 1938Anopheles mousinhoi de Meillon & Pereira 1940Anopheles njombiensis Peters 1955Anopheles seydeli Edwards 1929Group WellcomeiAnopheles distinctus Newstead & Carter 1911Anopheles erepens Gillies 1958Anopheles theileri Edwards 1912Anopheles wellcomei Theobald 1904subspecies ugandae Evans 1934subspecies ungujae White 1975subspecies wellcomei Theobald 1904Series Neocellia (Christophers 1924)
Anopheles ainshamsi Gad, Harbach & Harrison 2006Anopheles dancalicus Corradetti 1939Anopheles hervyi Brunhes, le Goff & Geoffroy 1999Anopheles jamesiiTheobald 1901Anopheles karwari* James 1903Anopheles maculipalpis Giles 1902Anopheles moghulensis Christophers 1924Anopheles paltrinierii Shidrawi & Gillies 1988Anopheles pattoni Christophers 1926Anopheles pretoriensis Theobald 1903Anopheles pulcherrimusTheobald 1902*Anopheles rufipes Gough 1910subspecies broussesi Edwards 1929subspecies rufipes Gough 1910Anopheles salbaii Maffi & Coluzzi 1958Anopheles splendidus Koidzumi 1920Anopheles theobaldi Giles 1901Complex StephensiAnopheles stephensi* Liston 1901Complex SuperpictusAnopheles superpictus* Grassi 1899Group Annularis (Reid 1968)Anopheles pallidus Theobald 1901Anopheles philippinensis* Ludlow 1902Anopheles schueffneri Stanton 1915Group Jamesii (Rattanarithikul et al. 2004)Anopheles jamesii Theobald 1901Anopheles pseudojamesi Strickland & Chowdhury 1927Anopheles splendidus Koidzumi 1920Group Maculatus (Rattanarithikul & Green 1987)Anopheles dispar Rattanarithikul & Harbach 1991Anopheles greeni Rattanarithikul & Harbach 1991Anopheles pseudowillmori Theobald 1910Anopheles rampaeAnopheles willmori James 1903Series Neomyzomyia (Christophers 1924)
Anopheles amictus Edwards 1921Anopheles annulatus Haga 1930Anopheles aurirostris Watson 1910Anopheles dualaensis Brunhes le Goff & Geoffroy 1999Anopheles hilli Woodhill & Lee 1944Anopheles incognitus Brug 1931Anopheles kochi Dönitz 1901Anopheles kokhani Vythilingam, Jeffery & Harbach 2007Anopheles kolambuganensis Baisas 1932Anopheles longirostris Brug 1928Anopheles mascarensis de Meillon 1947Anopheles meraukensis Venhuis 1932Anopheles novaguinensis Venhuis 1933Anopheles saungi Colless 1955Anopheles stookesi Colless 1955Anopheles watsonii Leicester 1908Complex AnnulipesAnopheles annulipes Walker 1856Complex LungaeAnopheles lungae Belkin & Schlosser 1944Anopheles nataliae Belkin 1945Anopheles solomonis Belkin, Knight & Rozeboom 1945Complex PunctulatusAnopheles clowi Rozeboom & Knight 1946Anopheles farauti* Laveran 1902Anopheles hinesorum Schmidt 2001Anopheles irenicus Schmidt 2003Anopheles koliensis Owen 1945Anopheles punctulatus Dönitz 1901Anopheles torresiensis Schmidt 2001Group ArdensisAnopheles ardensis Theobald 1905Anopheles buxtoni Service 1958Anopheles cinctus Newstead & Carter 1910Anopheles deemingi Service 1970Anopheles eouzani Brunhes le Goff & Bousses 2003Anopheles kingi Christophers 1923Anopheles machardyi Edwards 1930Anopheles maliensis Bailly-Choumara & Adam 1959Anopheles millecampsi Lips 1960Anopheles multicinctus Edwards 1930Anopheles natalensis Hill & Haydon 1907Anopheles vernus Gillies 1968Anopheles vinckei de Meillon 1942Group Kochi (Rattanarithikul et al 2004)Anopheles kochi Donitz 1901Group LeucosphyrusAnopheles baisasi Colless 1957Anopheles cristatus King & BaisasGroup Tessellatus (Rattanarithikul et al 2004)Anopheles tessellatus Theobaldsubspecies A. t. kalawara Stoker & Waktoedisubspecies A. t. orientalis Swellengrebel & Swellengrebel de Graafsubspecies A. t. tessellatus TheobaldSeries Paramyzomyia (Christophers & Barraud 1931)
Group CinereusAnopheles azevedoi Ribeiro 1969Anopheles cinereus Theobald 1901subspecies cinereus Theobald 1901subspecies hispaniola Theobald 1903Group ListeriAnopheles listeri de Mellion 1931Anopheles multicolor* Cambouliu 1902Anopheles seretsei Abdulla-Chan Coetzee & Hunt 1998Series Pyretophorus (Blanchard 1902)
Anopheles christyi Newstead & Carter 1911Anopheles daudi Coluzzi 1958Anopheles indefinitus Ludlow 1904Anopheles limosus King 1932Anopheles litoralis King 1932Anopheles ludlowae Theobald 1903subspecies ludlowae Theobald 1903subspecies torakala Stoker & Waktoedi 1949Anopheles parangensis Ludlow 1914Anopheles vagus* Dönitz 1902Complex Gambiae (White 1985)Anopheles arabiensis* Patton 1905Anopheles bwambae White 1985Anopheles comorensis Brunhes le Goff & Geoffroy 1997Anopheles gambiae* Giles 1902Anopheles melas* Theobald 1903Anopheles merus Dontiz 1902Anopheles quadriannulatus A Theobald 1911Anopheles quadriannulatus B Theobald 1911Complex Subpictus (Sugana et al. 1994)Anopheles subpictus* Grassi 1899Complex Sundaicus (Sukowati 1999)Anopheles epiroticus Linton & Harbach 2005Anopheles sundaicus* Rodenwaldt 1925Subgenus Kerteszia
Anopheles auyantepuiensis Harbach & Navarro 1996Anopheles bambusicolus Komp 1937Anopheles bellator* Dyar & Knab 1906Anopheles boliviensis Theobald 1905Anopheles cruzii* Dyar & Knab 1908Anopheles gonzalezrinconesi Cova Garcia, Pulido & de Ugueto, 1977Anopheles homunculus* Komp 1937Anopheles laneanus Corrêa & Cerqueira 1944Anopheles lepidotus Zavortink 1973Anopheles neivai Howard, Dyar & Knab 1913Anopheles pholidotus Zavortink 1973Anopheles rollai Cova Garcia, Pulido & de Ugueto 1977Note: Anopheles cruzii is known to be a species complex, but the number species in this complex has yet to be finalised.