Anopheles maculipennis Meigen, 1818.
Subfamily Anophelinae. A total of 508 formally recognised species and more than 50 unnamed members of species complexes are recognised as distinct morphological and/or biological species of the genus. The formally named species are placed in eight subgenera, Anopheles (206 species), Baimaia (1), Cellia (233), Christya (2), Kerteszia (12), Lophopodomyia (6), Nyssorhynchus (43) and Stethomyia (5). The three largest subgenera are further segregated into Sections, Series and Groups (see Anopheles Classification). Genus abbreviation – An.
Foster et al. (2017) proposed the elevation of Kerteszia, Lophopodomyia, Nyssorhynchus and Stethomyia from subgeneric status to generic status based on phylogenetic analyses of mitochondrial protein coding genes. Although the approach and results of the study are laudable, the justification for changing the rank of the four groups is weak, untenable and neglects to consider the consequences of the proposal. For example, in speaking with the first author of the paper, it is obvious that the authors failed to realise that the spelling of adjectival names (currently masculine as names of Anopheles) would have to be changed to agree in gender with the feminine Kerteszia, Lophopodomyia and Stethomyia. As the groups are fully diagnosable and no less manageable as subgenera, their elevation to generic status is clearly unnecessary, and the assertion that the change of status adds stability to the classification of Anophelinae is unsubstantiated. For these reasons, and because many workers in the applied and scientific communities are unlikely to accept the proposed generic rank of the four groups, their subgeneric status is retained herein. See further comments of Harbach (2018) and under Phylogenetic relationships below.
Most members of genus Anopheles are immediately recognised by their overall appearance. The majority of the adults are slender insects with the head and abdomen oriented in a straight line at an angle to the surface when at rest. The maxillary palpi are about as long as the proboscis and in males they are clubbed apically; the posterior margin of the scutellum is evenly rounded (distinction from Chagasia); vein M1+2 and vein M3+4 are straight or evenly curved, not sinuate (distinction from Bironella); and the abdominal segments usually have only small patches of scales or none at all (distinction from culicines). Larvae are immediately recognised by the absence of a siphon (distinction from culicines), the absence of palmate setae on the mesothorax (distinction from Bironella) and the absence of both uniquely developed palmate setae on abdominal segments III‒V and a fringe of setae on the posterolateral lobes of the spiracular apparatus (distinction from Chagasia). See Anophelinae.
Genus Anopheles is not demonstrably monophyletic with regard to genus Bironella and subgenera Lophopodomyia and Stethomyia. Subgenera Kerteszia, Nyssorhynchus and Cellia are monophyletic, and Kerteszia and Nyssorhynchus are sister taxa. The monophyly of the Sections and most Series of subgenera Anopheles, Cellia and Nyssorhynchus are doubtful. Based on analysis of a data set consisting of COI and COII mtDNA and 2.8S rDNA sequences (Freitas et al., 2015), subgenus Anopheles (10 species), as well as subgenera Cellia (25 species), Kerteszia (three species), Nyssorhynchus (six species) and Stethomyia (two species), were recovered as monophyletic clades. See review of Harbach (2007) and the evolutionary hypotheses of Harbach (2013) and Harbach & Kitching (2016).
Karimian et al. (2014) used sequences of COI mtDNA and ITS2 rDNA to investigate the phylogenetic relationships of the Anopheles species (15 and 28 respectively) that occur in the region of the Iranian plateau. The study included 16 species of subgenus Anopheles, 12 from the Anopheles Series and four from the Myzorhynchus Series; and 18 species of subgenus Cellia, eight from the Neocellia Series, six from the Myzomyia Series, three from the Paramyzomyia Series and one from the Pyretophorus Series. The monophyly of the subgenera was supported by the ITS2 data but not by the COI data when these were subjected to maximum parsimony analyses. The ITS2 data supported the integrity of the Series for the most part, but was not able to separate the one species of the Pyretophorus Series from the members of the Paramyzomyia Series.
Neafsey et al. (2015) constructed a maximum likelihood phylogeny for 18 species of subgenera Anopheles (two species), Cellia (14 species) and Nyssorhynchus (two species) from aligned protein sequences of 1,085 single-copy orthologs. The results, although taxon limited, support the monophyly of the three subgenera and indicate that the ancestral stem-group gave rise to Nyssorhynchus about 100 Mya and a lineage which later gave rise to Anopheles and Cellia. In contrast, Freirtas et al. (2015) (see above) inferred that genus Anopheles diverged from a common ancestor approximately 110 Mya. The results of Neafsey et al. convincingly support the monophyly of the Pyretophorus Series of subgenus Cellia and its emergence about 30 Mya. In agreement with the supposition of Reid & Knight (1961) that the monobasic subgenus Christya (as the Christya Series) is the “more primitive” group of subgenus Anopheles, the phylogenetic analyses of Harbach & Kitching (2016) indicate that this taxon is sister to all Anophelinae except genus Chagasia.
As noted above, Foster et al. (2017) proposed (suggested?) the elevation of subgenera Kerteszia, Lophopodomyia, Nyssorhynchus and Stethomyia to generic status based on phylogenetic analyses of mitochondrial protein coding genes. They also suggested the elevation of the Myzorhynchella Section of subgenus Nyssorhynchus to subgeneric status in their proposed genus Nyssorhynchus. The suggested actions are questionable in view of relationships portrayed in the authors’ featured phylogeny rooted on Chagasia, where the other groups of anophelines form a polytomy with three branches: (1) Stethomyia, (2) Lophopodomyia + Kerteszia and (3) Bironella + (Nyssorhynchus + (Cellia + Anopheles)). In view of the results of previous studies, both morphological and molecular (see above), and the paucity of Old World taxa included in the analyses, the relationships should be regarded with scepticism and changes to the current status of generic-level taxa should be avoided until significantly more molecular data are available to test, corroborate and further resolve relationships of the global diversity of Anophelinae. Also see the relationships of Anopheles generated in the phylogenetic analyses of Wang et al. (2015) based on 2,007 single-copy genes and Chu et al. (2018) based on mitochondrial genomes.
Anopheles larvae are adapted to a variety of aquatic habitats, but occur predominantly in ground waters. Some species require aerated water, others brackish water and some inhabit cavities such as tree holes (Plumbeus Group, subgenus Anopheles) and the axils of epiphytic plants (subgenus Kerteszia, except for An. bambusicolus which inhabits bamboo). Specific habitats contain stagnant water or water that is slowed down by vegetation or objects in specific niches occupied by the larvae. The larvae of all species feed at the water surface, where they attach to the surface film by the spiracular apparatus, palmate setae and special notched organs on the prothorax. They rotate the head 180° so that particles of food at the surface can be swept into the mouth by currents produced by the mouth brushes. The larvae generally rest with the end of the abdomen against objects and are therefore found in greatest numbers in areas with emergent vegetation at the margins of the habitats. The adults of most Anopheles are active at night (nocturnal) or during twilight periods (crepuscular), and rest in cool, damp places during the day. Blood-feeding is largely restricted to warm-blooded animals. Information on host specificity primarily pertains to those species that feed on humans and domestic animals. Females bite humans inside or outside houses. They normally fly no farther than 1‒3 km from the larval habitats.
Mosquitoes of genus Anopheles are the sole vectors of human malarial parasites. Some species are effective vectors of microfilariae and some may be involved in the transmission of encephalitis viruses. Anopheles are vectors of numerous animal pathogens, including species of malaria protozoa that do not affect humans. Presently, only the o’nyong-nyong virus is known to be consistently transmitted to vertebrates by Anopheles mosquitoes. However, a recent systematic review of the literature has revealed that at least 51 viruses have been isolated from species of Anopheles, many of which have the potential to cause febrile disease in humans or other vertebrates (Minkeu & Vernick, 2018).
Cellia is the largest subgenus with all species occurring in the Old World. The subgenus is segregated into six Series (Cellia, Neocellia, Myzomyia, Neomyzomyia, Paramyzomyia and Pyretophorus). Each series contains vectors of malarial protozoa and microfilariae. The most important malaria vectors include An. arabiensis, An. funestus, An. gambiae and An. moucheti in the Afrotropical Region; An. balabacensis, An. baimaii, An. culicifacies, An. dirus, An. latens, An. leucosphyrus, An. maculatus, An. minimus, An. fluviatilis s.l., An. sundaicus and An. superpictus in the Oriental Region; members of the An. farauti and An. punctulatus complexes in the Australasian Region; An. sergentii and An. stephensi in the Middle East and the Indian Subcontinent.
Subgenus Anopheles is also divided into six series, but only the Myzorhynchus and Anopheles Series contain vector species. Some primary vectors of historical and contemporary importance in the transmission of malaria protozoa include An. freeborni in western North America, An. sinensis in southeastern areas of the Palaearctic Region, An. atroparvus in Europe and eastern Asia, and An. pseudopunctipennis at higher elevations in Central and South America.
Subgenus Nyssorhynchus contain species that are variously distributed from Argentina to the southern USA. Anopheles albimanus, An. aquasalis, An. argyritarsis, An. darlingi and An. nuneztovari are vectors of malarial protozoa. Anopheles albitarsis and An. aquasalis also transmit arboviruses, and some species also transmit Wuchereria bancrofti.
Subgenus Kerteszia occurs in Central and South America. Six species are known to transmit malarial protozoa, but only An. bellator in Trinidad and An. cruzii in Brazil are important vectors. Anopheles bellator also transmits the helminths that cause Bancroftian filariasis.
Species of the remaining subgenera, Baimaia in the Oriental Region, Christya in the Afrotropical Region and Stethomyia and Lophopodomyia in the Neotropical Region, are not of medical importance to humans.
Anopheles has an almost world-wide distribution. Species of the genus occur in temperate, subtropical and tropical areas, but are absent from the majority of the Pacific Islands, including the large ones of New Zealand, Fiji and New Caledonia, and isolated islands in the Atlantic. Anopheles species are found at elevations from coastal areas to mountainous terrain.
Lane, 1953 (Neotropical Region); Mattingly & Knight, 1956 (Arabia); Cova-Garcia, 1961 (Venezuela); Belkin, 1962 (taxonomy, South Pacific); Forattini, 1962 (Neotropical Region); DuBose & Curtin, 1965 (keys, Mediterranean area); Grjebine, 1966 (Madagascar); Gillies & de Meillon, 1968 (Afrotropical Region); Reid, 1968 (Malaysia, Borneo); Belkin et al., 1970 (Jamaica); Cagampang-Ramos & Darsie, 1970 (keys, Philippine Islands); Zavortink, 1970 (tree hole species, world); Zavortink, 1973 (subgenus Kerteszia); Gutsevich et al., 1974 (former USSR); Harrison & Scanlon, 1975 (subgenus Anopheles, Thailand); Klein, 1977 (Cambodia); Faran, 1980 (Albimanus Section, subgenus Nyssorhynchus); Tanaka et al., 1979 (Japan); Wood et al., 1979 (Canada); Harrison, 1980 (Myzomyia Series, subgenus Cellia, Thailand); Darsie & Ward, 1981, 2005 (keys, North America); Faran & Linthicum, 1981 (subgenus Nyssorhynchus, Amazonia); Lu & Li, 1982 (China); Clark-Gil & Darsie, 1983 (Guatemala); Rao, 1984 (India); Lee et al., 1987 (Australasian Region); Gillies & Coetzee, 1987 (Afrotropical Region); Linthicum, 1988 (Argyritarsis Section, subgenus Nyssorhynchus); Das et al., 1990 (keys, India); Darsie & Pradhan, 1990 (Nepal); Wilkerson & Strickman, 1990 (keys, Central America and Mexico); Glick, 1992 (keys, southwestern Asia and Egypt); Peyton et al., 1992 (taxonomy, subgenera Kerteszia and Nyssorhynchus); Rattanarithikul & Panthusiri, 1994 (keys, medically important species, Thailand); Nagpal & Sharma, 1995 (India); Lu Baolin et al., 1997 (China); Harbach et al., 2005 (subgenus Baimaia); Rattanarithikul et al., 2006 (keys, Thailand); Harbach, 2007 (phylogeny); Azari-Hamidian & Harbach, 2009 (keys, Iran); Harbach, 2013 (classification and phylogeny); Harbach & Kitching, 2016 (subgeneric status of Christya, phylogeny); Freitas et al., 2015 (phylogeny); Gunathilaka et al., 2014 (key, larvae, Sri Lanka); Wang et al., 2015 (phylogeny); Gunathilaka, 2017 (key, adults, Sri Lanka); Foster et al., 2017 (phylogeny); Chu et al., 2018 (phylogeny); Poinar et al., 2019 (Priscoculex); Coetzee, 2020 (Afrotropical Region, keys); Irish et al., 2020 (Afrotropical Region, country distributions); Sallum et al., 2020a (South America, classification, bionomics, distributions); Sallum et al., 2020b (South America, fourth-instar larvae, morphology, key); Sallum et al., 2020c (South America, male genitalia, morphology, key); Sallum et al., 2020d (South America, adult females, morphology, key); Santos et al., 2022 (phylogenetic relationships).