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Open access peer-reviewed chapter
By Ralph E. Harbach
Submitted: February 20th 2012Reviewed: October 26th 2012Published: July 24th 2013
Anopheles was introduced as a genus of mosquitoes in 1818 by Johann Wilhelm Meigen , a German entomologist famous for his revolutionary studies of Diptera. Little was done on the taxonomy of Anopheles until the discovery during the last two decades of the 19th century that mosquitoes transmit microfilariae and malarial protozoa, which initiated a drive to collect, name and classify these insects. In 1898, the Royal Society and the Rt. Hon. Joseph Chamberlain, Secretary of State for the Colonies of Britain, appointed a Committee to supervise the investigation of malaria. On 6 December 1898, Mr. Chamberlain directed the Colonies to collect and send mosquitoes to the British Museum (Natural History) (Figure 1), and in 1899 the Committee appointed Frederick V. Theobald to prepare a monograph on the mosquitoes of the world, which was published in five volumes between 1901 and 1910 [2‒6]. As a consequence, many new generic names were introduced in an effort to classify numerous new mosquito species into seemingly natural groups. Theobald proposed 18 genera for species of Anopheles based on the distribution and shape of scales on the thorax and abdomen. Four of these proposed genera, Cellia, Kerteszia, Nyssorhynchus and Stethomyia, are currently recognized as subgenera of Anopheles and the other 14 are regarded as synonyms of one or other of subgenera Anopheles, Cellia or Nyssorhynchus. Theobald, however, was not the only person to propose generic names for species of Anopheles. During the first three decades of the 20th century, 37 genera (including the 18 recognized by Theobald) were established for species of Anopheles .
As additional new species were discovered, it became increasingly apparent that Theobald’s system of classification was neither practical nor natural. Frederick Knab in North America, one of the early critics of Theobald’s classification, stated that “the subject was made needlessly difficult by hasty work and by the sub-division of the old genus Anopheles into numerous ill-defined and fancifully differentiated genera. The intricacies of this ‘system,’ unwarranted from both a scientific and practical standpoint, even the trained entomologist could not tread with safety, and to others it could be no less than hopeless or disastrous” . Consequently, during the two decades following the completion of Theobald’s monograph in 1910, significant changes were made toward a much more conservative system of classification, culminating in the reduction of 38 genus-group names (including Anopheles) to the recognition of the single genus Anopheles.
The current subgeneric classification of Anopheles is based primarily on the number and positions of specialized setae on the gonocoxites of the male genitalia (Figure 2), and this basis of classification has been accepted since it was introduced by Sir (Samuel) Rickard Christophers in 1915 . Christophers proposed three generic subdivisions, which F.M. Edwards  and Francis Metcalf Root  formally recognized as subgenera Anopheles, Myzomyia (=Cellia) and Nyssorhynchus. Edwards adopted this system and added subgenus Stethomyia in his classical treatise on family Culicidae published in 1932 . This system recognized Kerteszia as an informal group within subgenus Nyssorhynchus. Kerteszia was elevated to subgeneric status by W.H.W. Komp . Subgenus Lophopodomyia was proposed by P.C.A. Antunes in 1937  and subgenus Baimaia was introduced by Ralph E. Harbach and his colleagues in 2005 .
Genus Anopheles currently includes 465 formally named species that are disproportionately divided between seven subgenera: Anopheles (cosmopolitan, 182 species), Baimaia (Oriental, one species), Cellia (Old World, 220 species), Kerteszia (Neotropical, 12 species), Lophopodomyia (Neotropical, six species), Nyssorhynchus (Neotropical, 39 species) and Stethomyia (Neotropical, five species) . Four of the subgenera, Anopheles, Cellia, Kerteszia and Nyssorhynchus, include the species that transmit human malarial parasites. Most vector species of Anopheles have been found to comprise complexes of sibling species.
The aim of classification is to group and categorize biological entities that share some unifying characteristics. Classification has been defined by Ernst Mayr & W.J. Bock  as “The arrangement of similar entities (objects) in a hierarchical series of nested classes, in which each more inclusive higher-level class is subdivided comprehensively into less inclusive classes at the next lower level.” These classes (groups) are known as taxa (singular: taxon). The level of a taxon in a hierarchical classification is referred to as a taxonomic rank or category. Ideally, taxonomic categories should denote equivalent phylogenetic rank; however, in practice they are basically subjective groupings of subordinate taxa that are presumed to represent monophyletic groups of species that are assigned to taxonomic ranks based on shared morphological and biological characteristics that are not a measure of phylogenetic equivalence. For this reason, the taxonomic categories of genus Anopheles, including the formal rank of subgenus, should not be considered to represent equivalent phylogenetic ranks.
Infrasubgeneric categories (taxonomic ranks below subgenus) have no formal status under the International Code of Zoological Nomenclature . They are convenience categories only, often based on superficial similarities that may not indicate natural relationships. The informal categories used in the classification of Anopheles include Sections, Series, Groups, Subgroups and Complexes (see Appendix 1).
Unlike formal taxonomic categories, which precede the name of the taxonomic unit, for instance family Culicidae, genus Anopheles and species gambiae, the names of informal taxonomic categories follow the name of the taxonomic unit, for example the Pyretophorus Series, Hyrcanus Group or Gambiae Complex, which are written in Roman (i.e. non-italic) script with the first letter capitalized. It should be stressed that both formal and informal taxonomic entities are conceptual constructs invented by taxonomists for the purpose of creating some order in the diversity of species. For example, the species gambiae and the Hyrcanus Group, which are human-conceived taxonomic concepts, cannot be observed as entities or visualized under a microscope.
The internal classification of genus Anopheles (between genus and species levels) is based primarily on the schemes proposed by Edwards , John A. Reid & Kenneth L. Knight , Alexis Grjebine , M.T. Gillies & Botha de Meillon , Reid , Michael E. Faran  and Kenneth J. Linthicum . These schemes were reviewed, amalgamated and updated in 1994  and updated again in 2004 and 2012 [27,16 respectively]. The three largest subgenera, i.e. Anopheles, Cellia and Nyssorhynchus, are divided into hierarchical systems of informal taxonomic categories (Appendix 1; examples shown in Figure 3). Subgenus Anopheles is divided into two Sections based on the shape of the pupal trumpet. The Laticorn Section was created for species with a wide funnel-shaped trumpet having the longest axis transverse to the stem, and the Angusticorn Section for species with a semi-tubular trumpet having the longest axis vertical more or less in line with the stem . Subgenus Nyssorhynchus is divided into three Sections based on unique combinations of larval, pupal and adult characters . Subgenus Cellia and the Sections of subgenera Anopheles and Nyssorhynchus are divided into Series, the larger Series are divided into species Groups, and some Groups are further divided into Subgroups and species Complexes. Most of the groupings at each level of classification are presumed to represent natural groups of species, thus implying phylogenetic relationships, but much additional basic taxonomic research is needed before the formal and informal taxa can be firmly established as monophyletic entities. The internal classification of the genus (subgenera and infrasubgeneric groups) is detailed in Appendix 1. An alphabetical list of all formally named, currently recognized species and their position in the classification is provided in Appendix 2. Similarly, all currently known sibling species complexes are listed in Appendix 3, and the unnamed and provisionally designated species of the complexes and their position in the classification are listed in Appendix 4.
Anopheles is undoubtedly the most studied and best known genus of mosquitoes, largely because of their great impact on human health. As vectors of causative agents of malaria and filariasis, Anopheles mosquitoes have affected the lives of more humans than any other insects. As a matter of fact, Anopheles is one of few groups of eukaryote organisms that have had an impact on human evolution ‒ the emergence of sickle cell anemia as a mode of resistance to malarial protozoa. As a result of more than a century of studies by medical entomologists, taxonomists and geneticists, 537 species of Anopheles are currently known and most have been formally named (87%) (Appendix 2), but until recently little work has been done to understand the evolution and phylogenetic relationships of these mosquitoes.
The phylogenetic studies of anopheline mosquitoes conducted to date are summarized in Appendix 5. In view of the impact of malaria on human health, it is not surprising that most of these studies have dealt with species Groups, Subgroups and Complexes that include vectors of human malarial protozoa. It is obvious that the evolutionary relationships of malaria vectors and their closest allies have received more attention than other groups. However, none of these studies can be regarded as complete in terms of taxonomic coverage of any group, and the field of disease vector systematics presents many opportunities for further research. Phylogenetic patterns are used to interpret bionomic features such as differences in the nature of blood-feeding by adult females, feeding behavior and the occurrence of immature stages in aquatic habitats.
Mosquitoes probably evolved in the Jurassic [12,29,30] (146‒200 Mya) -, along with the early mammals, first birds and first flowering plants. Unfortunately, due to the paucity of mosquito fossils, there is no direct indication of the evolutionary history of anopheline mosquitoes. The second oldest fossil mosquito, Paleoculicis minutus  from the Late Cretaceous (66.0–100.5 Mya), has morphological features that indicate a closer affinity with culicine than anopheline mosquitoes, which suggests that this ancestral lineage is younger than the lineage that gave rise to subfamily Anophelinae. Anopheles (Nyssorhynchus?) dominicanus  and An. (?) rottensis  are the only fossil anopheline mosquitoes. The former is from the mid-Tertiary (about 15–45 Mya) and the latter is from the Late Oligocene of Germany (approximately 25 Mya). If the anopheline mosquitoes are indeed ancestral to all other Culicidae [18,34], it would appear from available fossil evidence that extant groups may have evolved in the Cenozoic Era (<66.0 Mya). From divergence times based on sequence data for nuclear protein-coding genes and fossil calibration points, it appears that major mosquito lineages date to the Early Cretaceous (100.5–145.0 Mya), and the ancestral lineage of anophelines may have appeared as early as the Jurassic (~145 Mya) .
Anopheles is the nominotypical genus of subfamily Anophelinae. In addition to Anopheles (cosmopolitan), the subfamily includes two other genera: Bironella (Australasian) and Chagasia (Neotropical). Cladistic analyses of morphological data and DNA sequences of various ribosomal, mitochondrial and nuclear genes strongly support the placement of Chagasia in an ancestral relationship to all other anophelines [18,34‒41].
In 2000, Sallum et al.  performed the first phylogenetic analysis of subfamily Anophelinae, based on morphological characters. The results indicated that genus Anopheles is paraphyletic because it included genus Bironella. Subgenera Kerteszia, Nyssorhynchus, Cellia, Lophopodomyia and Stethomyia, along with genus Bironella, were found to be monophyletic taxa dispersed among various Series and species Groups of subgenus Anopheles. The Christya Series of subgenus Anopheles was placed with Kerteszia + Nyssorhynchus and this clade was sister to Cellia + all other anophelines except Chagasia.
Two years later, Sallum et al.  conducted a molecular analysis of anopheline relationships based on ribosomal (18S, 28S) and mitochondrial (COI, COII) DNA sequences. The results of that study cannot be compared directly with the results of their earlier study  because significantly fewer taxa were included in the analyses. Nevertheless, the molecular data corroborated the paraphyly of genus Anopheles relative to Bironella and the sister-group relationship of Kerteszia and Nyssorhynchus, and supported the monophyly of the other subgenera and genus Bironella, which was reconstructed as the sister to Lophopodomyia rather than Stethomyia.
In 2005, Harbach & Kitching  revised and expanded the phylogenetic analysis of Sallum et al. , with special consideration of the specialized setae of the male gonocoxites (Figure 2) that diagnose the subgenera. Parsimony analysis of the data set under implied weighting supported the monophyly of subgenera Cellia, Kerteszia and Nyssorhynchus, and the sister relationship of Kerteszia + Nyssorhynchus. Subgenus Anopheles was recovered as a polyphyletic lineage basal to a monophyletic clade consisting of Kerteszia + Nyssorhynchus and Cellia in a sister-group relationship. Bironella, Lophopodomyia and Stethomyia were firmly nested within subgenus Anopheles, which would be paraphyletic even if these taxa were subsumed within it. Subgenus Baimaia, represented by An. kyondawensis, was supported as the sister of Bironella + all other Anopheles. Bironella and Stethomyia, contrary to the earlier study of Sallum et al. , were also supported as monophyletic clades separate from subgenus Anopheles. The preferred cladogram of Harbach & Kitching (Figures 4 and 5) is taken here to represent the best available estimate of anopheline phylogeny and evolutionary relationships because it is based on a greater number of taxonomic groups and homologous characters than all other hypotheses published to date.
A later analysis of subgenus Anopheles by Collucci & Sallum  included 38 species representing the same Series (6) and species Groups (15) of the subgenus that were included in the study of Sallum et al. . The data were analyzed using successive approximations character weighting (SACW) and implied weighting (IW). Most of the relationships between members of the subgenus were either moderately or poorly supported. The Laticorn Section was recovered as a monophyletic clade in the IW analysis, suggesting that the laticorn development of the pupal trumpet is a derived condition for subgenus Anopheles. In the SACW analyses, members of the group comprised a paraphyletic lineage relative to the Cycloleppteron Series. The Angusticorn Section was recovered as a polyphyletic assemblage in both analyses. These results are contradicted by those of Sallum et al.  and Harbach & Kitching  who found that neither section is monophyletic. Below the section level of classification, only the Lophoscelomyia and Arribalzagia Series were recovered as monophyletic assemblages. The Myzorhynchus Series was paraphyletic relative to the Cycloleppteron, Christya and Arribalzagia Series, and the Anopheles Series was polyphyletic. Surprisingly, the two species of the Cycloleppteron Series included in the analyses were not grouped together, suggesting that the series is not monophyletic. In contrast, the Arribalzagia, Christya, Cycloleppteron, Lophoscelomyia and Myzorhynchus Series were recovered as monophyletic assemblages in the IW analysis of Harbach & Kitching (Figure 4). Furthermore, with the removal of subgenus Baimaia, the remaining species of the Anopheles Series included in their analysis also formed a monophyletic group. With the exception of the Pseudopunctipennis Group, all the species groups represented in the analysis of Collucci & Sallum (Aitkenii, Albotaeniatus, Culiciformis, Hyrcanus, Plumbeus, Umbrosus Groups) were recovered as monophyletic assemblages with moderate to strong support [the Pseudopunctipennis Group was also found to be polyphyletic in the study of Harbach & Kitching (Figure 4)]. The Hyrcanus Group was paired with An. coustani, which corroborates previous hypotheses of a close relationship between the Hyrcanus and Coustani Groups [20,36,40,43]. Unfortunately, the analyses of Collucci & Sallum are biased by the selection of outgroup taxa whose interrelationships with the ingroup taxa were unresolved in previous studies. Thus, the results of their study cast doubt on their assertion that subgenus Anopheles is monophyletic. Based on the relationships recovered by Harbach & Kitching, subgenus Anopheles would be monophyletic if subgenus Lophopodomyia were to be reduced to the status of a species Group of the Anopheles Series (Figure 4). The Anopheles Series is a morphologically diverse assemblage of species and informal taxonomic groups, a number of which at one time or another were deemed to merit recognition as subgenera . Sallum et al.  also found the Anopheles Series to be polyphyletic, but with its members interspersed in a complexity of inter-group relationships rather than arrayed in a pectinate sequence (Figure 4).
All phylogenetic studies conducted to date have demonstrated the monophyly of subgenera Cellia [36,38‒41], Kerteszia [36,38‒41,44] and Nyssorhynchus [36,38‒41], and the sister pairing of Kerteszia and Nyssorhynchus [36,40,41]. The sister relationship of Cellia and the two New World subgenera is not inconsistent with the molecular analyses of Sallum et al.  if Lophopodomyia + Bironella is excluded from the clade that contains Kerteszia + Nyssorhynchus, but it differs markedly from the results of their earlier study based on morphology and a larger number of taxa , which placed Kerteszia + Nyssorhynchus, along with An. implexus (Christya Series), in a sister-group relationship with Cellia + a clade comprised of Bironella, Lophopodomyia, Kerteszia and Nyssorhynchus. Anopheles implexus (Christya Series) is sister to the terminal clade formed by Kerteszia, Nyssorhynchus and Cellia in Figure 4.
Interpreting the current distributions of anophelines in an evolutionary context is problematic. The supercontinent of Pangaea existed in the Late Paleozoic and Early Mesozoic Eras from about 300‒200 Mya and gradually separated 200–145 Mya into the two supercontinents of Laurasia and Gondwana . As noted above, evidence from DNA sequence data and fossil calibration points  indicates that ancestral anophelines diverged from ancestral culicines about 217 Mya (230‒192 Mya), before the complete splitting of Pangaea. If this was the case, then the separation of Anopheles and Bironella about 54 Mya (75.8‒37.1 Mya, end of the Cretaceous to near the end of the Eocene Epoch of the Cenozoic)  must have occurred after the separation of Gondwana into multiple continents, i.e. Africa, South America, India, Antarctica and Australia, in the Cretaceous. Atlantica (the land mass that comprised present-day South America and Africa) separated from eastern Gondwana (the land mass that comprised Antarctica, India and Australia) 150‒140 Mya. South America started to separate from Africa in a south-to-north direction during the Middle Cretaceous (about 125‒115 Mya) . At the same time, Madagascar and India began to separate from Antarctica, and separated from each other 100‒90 Mya during the Cenomanian and Turonian Stages of the Late Cretaceous. India continued to move northward and collided with Eurasia about 35 Mya. Laurasia split to give rise to North America/Greenland and Eurasia about 60‒55 Mya. Africa began to move northeastward toward Europe and South America moved northward to separate from Antarctica. North and South America were joined by the Isthmus of Panama during the Pliocene, approximately 3.7‒3.0 Mya.
Belkin  hypothesized that anophelines initially differentiated in the American Mediterranean Region. In concert with this postulate, Harbach & Kitching  suggested a possible New World origin of subfamily Anophelinae based on the basal placement of Chagasia relative to Anopheles + Bironella in their phylogeny of mosquito genera. Based on a phylogeny of 16 anopheline species inferred from sequences of two protein-coding nuclear genes and the Neotropical distribution of Chagasia and four of the seven subgenera of Anopheles, Krzywinski et al.  agreed with the hypothesis that South America was the center of origin of Anophelinae. However, as will be seen below, more recent studies suggest a different scenario for the evolution of the extant groups of the subfamily. This scenario closely reflects Christophers  insightful observations:
Subgenus Anopheles appears to be the oldest of the predominant subgenera, not only on [morphological grounds], but by reason of its worldwide distribution and the greater diversity and distinctness of its forms; almost every species of the subgenus appears to be as distinctive as are the species groups of subgenus Myzomyia [=Cellia], if not more so.
Nyssorhynchus appears to be a Neotropical development from some pre-Anopheles form, whilst the group Arribalzagia appears to be a highly specialized development of subgenus Anopheles.
Myzomyia shows every evidence of being a new and actively disseminating branch, as is suggested by its complete absence from the New World. Had it been once disseminated throughout North America it is unlikely that it would have been eliminated from the whole continent so completely as to leave not a single species in this area, though there is no actual proof that this did not occur. The apparent affinity between the group Neomyzomyia and subgenus Nyssorhynchus suggests an intermediate ancestor, though not necessarily one in the south, i. e., such affinity does not prove or suggest a land-connection between Australia and South America, as the common ancestor may have been derived from the north and later eliminated. [next paragraph omitted]
The date of isolation of South America, judging by the history of mammals, would be from the middle of the Eocene, when connections between North and South America were severed, until the end of the Pliocene (Zittel). The anopheline fauna, therefore, arose from elements which pre-dated this period, and there were already subgenus Anopheles-like forms, as well as some earlier type from which Nyssorhynchus arose.
At some unknown period a similar special development took place, resulting in an early form (Neomyzomyia) of subgenus Myzomyia. This form appears to have once been distributed throughout the Oriental, Ethiopian [i.e. Afrotropical], and Australian Regions, and to have later undergone some regression, eventually remaining in greatest strength in the Australian Region.
Edwards, in reviewing the fossil remains of mosquitoes, notes that probably all the main divisions of the family [Culicidae] existed in Mid-Tertiary much as they do today, and with almost identical characters, and considers that, though no fossil Anopheles have been found, there can be no doubt from its morphology that this is also an old genus, probably older than any culicine form.
Based on the relationships shown in Figure 4, distributions of the principal group taxa (Appendix 6) and the geological dates listed above, it would appear that the ancestral lineage of Anopheles existed before the breakup of Pangaea and subsequently diversified into the modern subgenera and species after the separation of the continents. This would explain the cosmopolitan distribution and greater diversity of subgenus Anopheles, but not the earlier divergence of genus Chagasia and subgenus Stethomyia, which are confined to the Neotropical Region, the Oriental subgenus Baimaia and the Australasian genus Bironella (Figure 4). Chagasia possess several features that characterize species of subfamily Culicinae, including the strongly arched mesonotum, trilobed scutellum (Figure 6) and setae on the postpronotum. Based on these shared features, Chagasia has been considered an ancient group showing affinities with non-anophelines and phylogenetic analyses of morphological data and DNA sequences of various ribosomal, mitochondrial and nuclear genes strongly support its placement in an ancestral relationship to all other anophelines [33,35‒41]. From the foregoing, however, it is inferred here that Chagasia, with only seven species, is a relic of a once more widely distributed taxon that is now confined to residual areas of South and Central America. It is also possible, although less likely, that Chagasia, as suggested by the late John N. Belkin for other mosquitoes , may have originated through hybridization between early anopheline and culicine forms. Similarly, Bironella (as suggested by Christophers ), Baimaia and Stethomyia, with few species and restricted distributions, are also the remnants of once much more widely distributed forms. The isolation of ancestral members of subgenus Anopheles in South America also explains the uniqueness of the extant Neotropical fauna of the subgenus, especially the well-differentiated Arribalzagia Series. In accordance with this hypothesis, the following groups are also probably residual elements of once more widely distributed ancestral forms of subgenus Anopheles: the Afrotropical Christya Series (two species), the Australasian Atratipes (two species) and Stigmaticus (six species) Groups, the Oriental Alongensis (two species) and Culiciformis (three species) Groups, the Oriental Lophoscelomyia Series (five species) and the Neotropical Cycloleppteron Series (two species). It is noteworthy that the extant members of the relict groups are not vectors of human malarial parasites.
As noted previously, subgenus Anopheles has an almost world-wide distribution. Species are found at elevations from coastal areas to mountainous terrain 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. The sole species of subgenus Baimaia has been found only in forested hilly and mountainous areas between 14° and 17° north on either side of the Thai-Myanmar border and at a location near the Thai-Laos border in Thailand, and is probably also a relict taxon that has retained generalized ancestral features of the male genitalia . Most species of subgenus Cellia have distributions in the Afrotropical, Australasian and Oriental Regions, but some species occur in southern areas of the Palaearctic. Species of Cellia are conspicuously absent from the majority of the islands of the Pacific, including New Zealand, Fiji and New Caledonia. Species of subgenus Kerteszia are found in the Neotropical Region, from Veracruz State in Mexico through Central America and Atlantic South America, along the Andes and along the coast, to the States of Misiones in Argentina and Rio Grande do Sul in Brazil, and also occur south along the Pacific Coast of South America to the State of El Oro, Ecuador. The subgenus is absent from all islands of the West Indies except Trinidad, and from most of the vast expanse of the Amazon basin in South America . Species of subgenus Lophopodomyia are known to occur in areas of Panama and northern South America (Brazil, Colombia, Ecuador, French Guiana and Venezuela). Species of subgenus Nyssorhynchus are restricted to the Neotropical Region, except for An. albimanus, which extends into the Nearctic Region (northern Mexico and along the Rio Grande River in Texas). Finally, species of subgenus Stethomyia principally occur in southern Central America (Costa Rica and Panama) and northern South America (Brazil, Colombia, French Guiana, Guyana, Suriname and Venezuela), but one or two species are known to occur on the islands of Trinidad and Tobago and as far south as Peru and Bolivia.
Subgenera Kerteszia, Lophopodomyia, Nyssorhynchus and Stethomyia, and the Arribalzagia and Cycloleppteron Series of subgenus Anopheles are special to the Neotropical Region, where they probably originated following the separation of South America and Africa. The derived position of subgenera Cellia and Kerteszia + Nyssorhynchus relative to subgenus Anopheles (Figure 4) supports the hypothesis that the stem lineage of these subgenera originated in Gondwana and diverged following the separation of Atlantica to give rise to Cellia in Africa and Kerteszia and Nyssorhynchus in South America. It is interesting to note that Lophopodomyia and the Pseudopunctipennis Group are sister taxa in Figure 4, which is plausible in view of the hypothesized evolution of these groups from Neotropical ancestors. The Pseudopunctipennis Group is nearly restricted to the Neotropics, except for An. franciscanus and a minor extension of An. pseudopunctipennis into the Nearctic Region, which undoubtedly occurred relatively recently, after the land bridge formed to connect North and South America 3.7‒3.0 Mya. Except for these two species, all Anopheles species in the Nearctic Region are members of the Anopheles Series of subgenus Anopheles. Half of the species of the Holarctic Maculipennis Group (24 species) occur in the Nearctic Region and the other half occur in the Palaearctic. This indicates that the Maculipennis Group must have evolved in the Northern Hemisphere prior to the separation of North America and Eurasia during the Paleocene and Eocene Epochs (60‒55 Mya). The Plumbeus Group includes species in the Nearctic (2), Neotropical (4) and Palaearctic (3) Regions. Its position in the cladogram shown in Figure 4 is based on An. judithae, a Nearctic species. This group may be what paleontologists call a “stem group” , a paraphyletic or polyphyletic assemblage of species that share features of extinct taxa. The spotted distribution of these “living fossil” species suggests that their extinct relatives, ancestral forms of the Anopheles Series, existed before the separation of Pangaea. This bodes well with Christophers & Barraud’s 1931 hypothesis  that the eggs of species of the Plumbeus Group are primitive compared to other species of subgenus Anopheles.
Species in subgenus Cellia are confined to the Eastern Hemisphere, with members in the Afrotropical, Australasian, Oriental and Palaearctic regions (Figure 5, Appendix 6). The Afrotropical Region is characterized by a large number of species of subgenus Cellia and relatively few species of subgenus Anopheles. The Myzomyia Series is especially dominant, but species of the Neocellia, Neomyzomyia and Pyretophorus Series also occur in the region. The Myzomyia, Neocellia and Pyretophorus Series are represented in the Afrotropical and Oriental Regions, but no species, species groups or subgroups of these series (with the exception of the Minimus Subgroup) are common to both regions (see Appendix 6). The Myzomyia Series is a dominant group in Africa, where An. funestus is a principal malaria vector [52,53]. Related species of the Funestus Group, including An. minimus and other members of the Minimus Subgroup, are major vectors of malarial parasites in southern Asia [52,54]. Evidence from phylogenetic analyses of mitochondrial DNA (ITS2 and D3 sequences) indicates that the Funestus Group originated in the Afrotropical Region . The Neocellia Series also includes several important malaria vectors in southern Asia, notably An. stephensi and members of the Maculatus Group [52,54]. The Pyretophorus Series includes the formidable malaria vectors of the Gambiae Complex in Africa and important vectors of the Sundaicus and Subpictus Complexes in Southeast Asia [53,54]. The morphology-based phylogeny of Anthony et al.  indicates that the Pyretophorus Series originated in Africa and suggests that the capacity to vector malarial parasites is an ancestral condition subsequently lost independently in several lineages.
The anopheline fauna of the Australasian Region also shows evidence of isolation, but not to the degree indicated by the Neotropical fauna. The isolation appears to be more recent, corresponding to the separation of Australia from Antarctica between 37.0‒33.5 Mya. The region includes a preponderance of species of the Neomyzomyia Series of subgenus Cellia, which may signal a relatively recent arrival from the Oriental Region, with some diversification. Members of the Neomyzomyia Series are the only Anopheles in the South Pacific . Species groups of the series are confined to the Afrotropical (Ardensis, Mascarensis, Pauliani, Ranci, Rhodesiensis and Smithii Groups), Australasian (Punctulatus Group, Lungae Complex and unassigned species) or Oriental Region (Kochi, Leucosphyrus and Tessellatus Groups) (Appendix 6). The Neomyzomyia Series has been regarded as the most primitive series of subgenus Cellia based on egg morphology and the reduced or non-existent cibarial armature of females [57‒59], and is thought to have originated in Africa and subsequently disperse eastward to the Oriental and Australasian Regions [52,59]. None of the African species of the Neomyzomyia Series, except for An. nili, are major vectors of malaria. In comparison, most species of the Oriental Leucosphyrus and Australasian Punctulatus Groups of the Neomyzomyia Series are important vectors of both primate and human malarial parasites. The Cellia and Paramyzomyia Series of subgenus Cellia are restricted to the Afrotropical Region, except for An. pharoensis (Cellia Series) and An. multicolor (Paramyzomyia Series) which occur in adjacent arid areas of the Palaearctic (Sahara and Middle East). It seems reasonable to hypothesize that those series that are presently represented by groups in the Afrotropical, Australasian and Oriental Regions arose before eastern Gondwana (Antarctica, India and Australia) fragmented. The Mascarensis, Pauliani and Ranci Groups are confined to Madagascar, which supports the hypothesis that the ancestral forms of at least these groups of the Neomyzomyia Series existed before Madagascar separated from India 100‒90 Mya.
Human malaria probably evolved in Africa along with its mosquito hosts and other primates. Modern humans arose in Africa about 200,000 years ago and dispersed into Eurasia , reaching Australia about 40,000 years ago. Migration into the New World occurred about 15‒20 millennia ago, and most of the Pacific Islands were colonized by four thousand years ago. The point here is that the rise and dispersal of modern humans occurred long after the formation of the continents and the evolution of the major groups of Anopheles. Consequently, it seems reasonable to assume that human malarial parasites accompanied humans during their migration out of Africa and were passed on to species of Anopheles in other regions that had the ecological, physiological and behavioural attributes required to propagate infections and maintain transmission. These taxa were surely already adapted to feeding on primates, including the ancestors of Homo sapiens, and were capable of developing and transmitting the Plasmodium species specific to those hosts.
Comprehensive information on the dominant malaria vectors of the world, most of which are presumably recently evolved members of sibling species complexes (Appendix 3), is summarized in a series of publications (and a chapter of this book) by M. Sinka and a team of regional experts and technical advisors ‒ the Americas , Africa, Europe and the Middle East , the Asia-Pacific Region  ‒ that culminated in a thorough review of the principal malaria vector taxa of the world . At present, 96 formally named species of Anopheles are members of 26 sibling species complexes (Appendix 4). Twenty of these nominal species actually consist of more than one species, which all together comprise a total of 67 species. Excluding the name-bearing type species, the 58 species, plus five other unnamed species that are not members of species complexes, a total of 72 species, have yet to be given formal Latin names (Appendix 4).
A more robust phylogeny of Anopheles mosquitoes than is currently available may be of use in the fight against malaria. Foley et al.  suggested that it may help “by elucidating descent relationships of genes for refractoriness, insecticide resistance, and genetically determined ecological and behavioral traits important to malaria transmission.” Interrupting the life cycle of malarial parasites by genetically manipulating vector receptiveness to infection is a potential approach to malaria control. A natural classification of Anopheles predictive of biological and ecological traits could facilitate the manipulation of vector genomes by informing the dynamics of introduced genes. Obviously, co-evolutionary studies of parasites and vectors require phylogenies for the mosquitoes. This must far exceed the taxon-limited (exemplar-based) studies conducted to date as they do not provide a basis for gaining insights into interspecific and co-evolutionary relationships of vectors and parasites.
It seems fitting to end here with a comment concerning interspecific hybridization, which was mentioned above in relation to genus Chagasia in the Neotropical Region. Although anopheline species occur in sympatry in most ecosystems, hybridization has only been detected at very low levels between certain members of species complexes in subgenus Cellia, e.g. An. gambiae with both An. arabiensis and An. bwambae in Africa [63,64], An. dirus and An. baimaii in Thailand  and An. minimus and An. harrisoni in Vietnam . However, as advocated by Belkin , hybridization could provide sufficient genetic variation to permit adaptation to new habitats. Hybridization may occur regularly between some species, particularly widely distributed species that are morphologically similar. It could have played a role in the speciation and evolution of Anopheles mosquitoes and the pathogens they transmit.
Alphabetical list of formally named species of Anopheles and their position in the classification of the genus. For species Complexes, see Appendices 3 and 4; for authorship of species, visit http://mosquito-taxonomic-inventory.info/valid-species-list.
Sibling species complexes of Anopheles – formally named and unnamed species. The Maculatus, Maculipennis and Punctulatus Complexes are now considered to be super-complexes referred to as “Groups” with subordinate complexes. Likewise, the Culicifacies Complex is considered to be a Subgroup.
Unnamed and provisionally designated members of species complexes and their position in the classification of genus Anopheles (Sections of subgenera Anopheles and Nyssorhynchus are omitted). Excluding nominotypical members, the list includes 72 species that require formal Latin names.
|albitarsis sp. F,G,H,I||[114,115]||Nyssorhynchus||Albitarsis||Albitarsis||Albitarsis|
|annularis sp. A,B||||Cellia||Neocellia||Annularis||Annularis|
|annulipes sp. A‒Q||||Cellia||Neomyzomyia||Annulipes|
|Anopheles CP Form||||Nyssorhynchus||Oswaldoi||Oswaldoi||Strodei|
|barbirostris clades I‒IV||||Anopheles||Barbirostris||Barbirostris||Barbirostris||Barbirostris|
|benarrochi sp. B||||Nyssorhynchus||Oswaldoi||Oswaldoi||Strodei||Benarrochi|
|crucians sp. A‒E||||Anopheles||Anopheles||Punctipennis||Crucians|
|cruzii sp. A,B,C||||Kerteszia|
|culicifacies sp. A‒E||||Cellia||Myzomyia||Funestus||Culicifacies||Culicifacies|
|farauti sp. 4,5,6||[109,119]||Cellia||Neomyzomyia||Punctulatus||Farauti|
|fluviatilis sp. S,T,U||||Cellia||Myzomyia||Funestus||Minimus||Fluviatilis|
|gigas s.l. (Thailand)||||Anopheles||Anopheles||Lindesayi||Gigas|
|janconnae, lineage nr||||Nyssorhynchus||Albitarsis||Albitarsis||Albitarsis|
|longipalpis Type A||||Cellia||Myzomyia||Funestus||Minimus|
|longipalpis Type C||||Cellia||Myzomyia||Funestus||Funestus|
|marajoara lineages 1,2||||Nyssorhynchus||Albitarsis||Albitarsis||Albitarsis|
|nivipes (2 cytotypes)||||Cellia||Neocellia||Annularis||Nivipes|
|nuneztovari sp. A||||Nyssorhynchus||Oswaldoi||Oswaldoi||Oswaldoi||Nuneztovari|
|punctulatus, sp. nr||||Cellia||Neomyzomyia||Punctulatus|
|quadriannulatus sp. B||||Cellia||Pyretophorus||Gambiae|
|subpictus sp. A‒D||||Cellia||Pyretophorus||Subpictus||Subpictus|
|sundaicus sp. B‒E||[98,128]||Cellia||Pyretophorus||Ludlowae||Sundaicus|
|superpictus sp. A,B||[110,129]||Cellia||Neocellia||Superpictus|
|triannulatus sp. C||||Nyssorhynchus||Oswaldoi||Triannulatus||Triannulatus|
Phylogenetic studies of Anopheles mosquitoes. Groups included in the table are those recognized herein. None of the studies included all taxa that comprise the group investigated, but those marked with an asterisk (*) included the majority of species. Nucleotide sequences include COI, COII, cyt b, ND4, ND5 and ND6 from mitochondrial DNA (mtDNA); D2, D3, 18S, ITS1 and ITS2 from ribosomal DNA (rDNA); EF-1α, G6pd and white from nuclear DNA.
|cyt b, ND5, D2|
ND5, D2, G6pd, white
COI, COII, D2
|Freeborni and Quadri-|
|ITS2, COI, COII|
|Funestus Group||ITS2, COII, D3|
ITS2, COII, D3, ND5
|Maculatus Group||ITS2, COII, D3||[149–151]|
|ITS2, COI, COII, EF-1α|
ITS2, D2, COI, ND4
cyt b, ITS2, COI
|Myzorhynchella Section||ITS2, COI, white|||
Summary of the formal and informal group taxa (species complexes omitted) of genus Anopheles. The zoogeographic distribution and the number of formally named and informally designated species (in parentheses) are given for each taxon. Minor extensions of one or more species of a group into an adjacent zoogeographic region are disregarded. C = cosmopolitan; NW = New World; OW = Old World; Af = Afrotropical; Au = Australasian; Ne = Nearctic; Nt = Neotropical; Or = Oriental; Pa = Palaearctic.
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