Aedes (Stegomyia) aegypti (Linnaeus)

Harbach, Ralph E. & Wilkerson, Richard C., 2023, The insupportable validity of mosquito subspecies (Diptera: Culicidae) and their exclusion from culicid classification, Zootaxa 5303 (1), pp. 1-184 : 48-50

Aedes (Stegomyia) aegypti (Linnaeus)

subspecies aegypti ( Linnaeus, 1762) —original combination: Culex aegypti . Distribution: Worldwide tropics and subtropics ( Mattingly 1957b; Huang 2004; Powell et al. 2018; Soghigian et al. 2020) [see postscript note regarding current nomenclature].

subspecies formosus ( Walker, 1848) —original combination: Culex formosus (subspecific status by Mattingly 1957b). Distribution: Sub-Saharan Africa ( Mattingly 1957b; Huang 2004; Powell et al. 2018; Soghigian et al. 2020).

It is apropos here to reiterate what we advocated in the Introduction, i.e. we follow the definitions of species and subspecies of de Queiroz (1998, 1999, 2005a, 2005b, 2007, 2020, 2021). Herewith, a brief taxonomic conspectus of Ae. aegypti aegypti and Ae. aegypti formosus is provided, followed by some examples of how formosus fits as an incompletely separated lineage.

Aedes aegypti aegypti and Ae. aegypti formosus are members of the Aegypti Group ( Huang 2004), which also includes Ae. mascarensis ( MacGregor, 1924) , type locality Mauritius, an island nation in the Indian Ocean located about 800 km east of Madagascar, and Ae. pia Le Goff & Robert, 2013 (in Le Goff et al. 2013), type locality Mayotte, officially the Department of Mayotte, an Overseas Department of France in the Comoro Archipelago in the Indian Ocean located between Madagascar and Mozambique.

Using three molecular datasets, Soghigian et al. (2020) “found that: (a) the Aegypti Group diverged 16 MYA (95% HPD: 7–28 MYA) from its nearest African/Asian ancestor; (b) SWIO [Southwest Indian Ocean] populations of Ae. aegypti are basal to continental African populations; (c) after diverging 7 MYA (95% HPD: 4–15 MYA) from its nearest formally described relative (Ae. mascarensis ), Ae. aegypti moved to continental Africa less than 85,000 years ago, where it recently (<1,000 years ago) split into two recognized subspecies, Ae. aegypti formosus and a human commensal, Ae. aegypti aegypti ...”. The latter invaded the New World about 500 years ago via ships involved in the slave trade, and from there it invaded Asia about 150 years ago ( Gloria-Soria et al. 2016). Soghigian et al. also noted that “ Ae. pia is clearly the most distantly related and thus serves as an outgroup in [their] later analyses.” They also refer to Ae. aegypti in Madagascar as ‘ aegypti ’ Madagascar due to its large genetic distance from global aegypti sensu stricto and Ae. mascarensis from Mauritius.

Mattingly (1957b) considered three forms of aegypti sensu lato.

1. A. aegypti sens. str., the type form [worldwide tropics]. This form is variable in depth of colour but always either distinctly paler and browner (at least in the female) than the blackish African subspecies which is next described, or with pale scaling on the first abdominal tergite [terga], or both. In the type form extensions of pale scaling, if any, are limited either to bleaching of the two dark areas on the back of the head, or to the presence of pale scaling on the first abdominal tergite, or to both in combination.

2. A. aegypti ssp. formosus (Walker) [presumably retrieved from synonymy with aegypti in this cited publication]. This is a geographically representative form confined to Africa south of the Sahara, where it is the only form known to occur, except in coastal districts and in one or two areas of limited inland penetration. It is therefore designated as a subspecies. The name formosus was the first to be applied to any form occurring in the area ( Walker, 1848). The type, a female from Sierra Leone, is in the British Museum. It is in poor condition but there is nothing about either it or Walker’s description which would suggest either of the paler forms [the type form, above, and queenslandensis, below]. This subspecies differs from the type form in the markedly blackish appearance of the dark areas of the thorax and abdomen and in entirely lacking any bleaching or extension of pale scaling on any part of the body. It never has any pale scales on the first abdominal tergite.

A third form discussed by Mattingly, A. aegypti var. queenslandensis Theobald, 1901a [as Stegomyia fasciata variety] was later synonymized with aegypti sensu stricto by Huang (1979) and shown to be genetically indistinguishable from nominotypical aegypti in Australia ( Rašić et al. 2016).

It is hypothesized that nominotypical aegypti evolved in sub-Saharan Africa from a forest species utilizing natural containers for larval development, and then diverged into two forms, one remaining adapted to forest habitats ( Aedes aegypti formosus ) and the other adapted to primarily seek human hosts and to utilize artificial containers provided by humans ( Aedes aegypti aegypti ). Significantly, McBride et al. (2014) found a genetic change in an odorant receptor responsible for the change to a preference for human blood.

A few examples of differences between aegypti and formosus follow, many demonstrating incomplete lineage separation. Note that most work comparing aegypti and formosus in Africa has been carried out in East Africa, while the type locality of formosus is in West Africa ( Sierra Leone). Also note that despite the medical importance of aegypti and formosus , morphological studies of all stages have only been carried out on the invasive form in the New World and Asia. No detailed comparisons, other than documentation of adult abdominal markings, have been done for larvae and pupae of African aegypti or formosus , and therefore there are no comparisons with populations outside of Africa either.

McClelland (1974) scored pale abdominal markings of Ae. aegypti sensu lato worldwide in relation to biology using an artificial “paleness” scoring scheme. He found continuous intra- and interpopulation variation and determined that identification was not reliable using abdominal markings, i.e. there were discernible but no discrete groupings. He pointed out that part of the problem of correlating markings with habitat was imprecise terminology, and gave the example of “The same population of mosquitoes regarded as ‘feral’ when breeding in a forest would become ‘peridomestic’ if it persisted after a human settlement arose in the forest and ‘urban’ if the village grew to a town.” He then provided a list of what he considered to be more usable terms. In conclusion he stated: “I would venture further that A. aegypti comprises two species or incipient species. The pale or synanthropic species competitively excludes the dark or feral species from habitats where water and man are continuously present. The reverse occurs in habitats where most breeding sites are filled naturally by rainfall.”

Scott & McClelland (1975), using starch gel electrophoresis and specimens from eastern Kenya, stated: “The indoor and outdoor ecotypes differed considerably at three loci.” In the laboratory, caged indoor and outdoor ecotypes mated freely, but they stated: “We have demonstrated partial reproductive isolation between them; therefore, what we are calling two ‘ecotypes’ may actually be incipient species, partially isolated by habitat selection.”

Paterson et al. (1976) concurred with Scott& McClelland (1975),stating that “the data on the alkaline phosphatase and protein loci... are sufficient to eliminate the possibility that we are dealing with a single polymorphic species. In fact, the data for these two loci provide strong evidence for the existence of positive assortative mating in the field, thus supporting the view that they are distinct genetic species.”

Moore (1979), based solely on laboratory crossing experiments, determined that data for aegypti and formosus from Kenya were “consistent with the contention that Aedes aegypti is a single polytypic species.” We note that laboratory mating experiments with closely related, perhaps currently diverging species, probably do not reflect what is happening in nature.

Tabachnick et al. (1979), in a larger study of aegypti and formosus , also using starch gel electrophoresis and specimens from (eastern) Kenya, were ambiguous in their judgement of the status of the two forms. They stated: “The results suggest that gene flow between the two forms is restricted. None of the loci examined in this study provided evidence for the complete absence of gene flow between forms. We feel that, at present, the two forms can still be thought of as members of the same polytypic species. However, due to the distinct behavioral differences characteristic of each, and the evidence for restricted gene flow, speciation may be a likely eventuality.”

Lounibos (1981) studied the larval ecologies of mosquito species at two sites near the Kenyan coast (Rabai Location, Kilifi District and Shimba Hills National Park, Kwale District). Aedes aegypti larvae [sensu lato] were found in cultivated and ecotonal macrohabitats, predominantly in large tree holes and bamboo. Lounibos also noted that 96% of the Ae. aegypti collected for his study of tree holes and other natural containers corresponded to the morphologically dark subspecies formosus , as characterized by Mattingly (1957b). Most research on the two nominal taxa has been carried out on East African populations. In one study, in contrast to discrete local partitioning of the two forms in Kenya, Sylla et al. (2009), working in Senegal in West Africa, found a clear northwest to southeast cline in change in the proportions of individuals fitting the concept of aegypti versus formosus —in the northwest significantly more aegypti , in the southeast many more formosus . Vector competence measures also followed this cline but molecular genetic measures did not. The authors, however, pointed out many uncontrolled variables in the relatively small study.

Jupp et al. (1991) concluded “that in South Africa, Ae. aegypti is a single polymorphic species showing a considerable amount of variation in the degree of white scaling on the first two abdominal tergites [terga]. The presence of some rural sylvan non-anthropophilic populations in our country... might, however, indicate incipient speciation.”

Brown et al. (2011) used polymorphic microsatellite markers to test worldwide populations. They “identified two distinct genetic clusters: one included all domestic populations outside of Africa and the other included both domestic and forest populations within Africa. This suggests that human association in Africa occurred independently from that in domestic populations across the rest of the world. …Interestingly, two forms identified as subspecies aegypti and formosus were shown to coexist in a few places along the coast of East Africa, including the Rabai district of Kenya... where the former bred inside homes in villages and the latter bred in surrounding forests.” Three years later, Brown et al. (2014) “used DNA sequences of four nuclear genes and 1504 single nucleotide polymorphism (SNP) markers developed with restriction-site associated DNA (RAD) sequencing to test the hypothesis that Ae. aegypti originated in Africa, where a domestic form arose and spread throughout the tropical and subtropical world with human trade and movement.”

In Sudan, Abuelmaali et al. (2021) and Elnour et al. (2022) both reported geographically separated populations of a. formosus (in the west) and a. aegypti (in the east). Elnour et al. (2022) wrote that “Analysis supports a scenario in which Ae. aegypti entered Sudan on at least two independent occasions nearly 70–80 years ago.” We think this raises the possibility of interesting scenarios as aegypti reinvades localities in Africa. For example, if a. formosus evolved into a proto- a. aegypti and then into a. aegypti (see Powell et al. 2018), which then invaded the rest of the world, where is a. aegypti in Africa and how is it evolving in relation to the invasive a. aegypti in the rest of the world? Powell & Tabachnick (2013) stated that a. aegypti , as it occurs in the New World, is not known in West Africa today, except perhaps as a reintroduction into ports ( Brown et al. 2011).

We think there is abundant evidence concordant with the subspecies concept of de Queiroz (2020) to hereby elevate formosus to its original specific status: Aedes (Stegomyia) formosus ( Walker, 1848) . Aedes formosus is currently listed as a species in the Encyclopedia of Life.

The following nominal forms are currently listed as synonyms of Aedes aegypti in Wilkerson et al. (2021). Many will remain in doubt until existing types are examined to see if any correspond to Ae. formosus . Some of these are probably from a now extinct Mediterranean (North African, European) distribution of what was thought to be reintroduced Ae. aegypti from the New World ( Powell et al. 2018). There are also New World synonyms, which are probably Ae. aegypti , but verification is needed since it is possible that Ae. formosus is present in the New World. Given the unusual biogeography of the Madagascar area, and predictions of undescribed taxa by Soghigian et al. (2020), synonyms from Madagascar and Mauritius also require further scrutiny. African synonyms could potentially be Ae. agypti or Ae. formosus .

Unless otherwise indicated, * = Mediterranean, † = New World, + = Madagascar and Mauritius and # = Africa in the following list of current synonyms of Aedes aegypti : * Culex argenteus Poiret, 1787 ; † Culex fasciatus Fabricius, 1805 ; * Culex calopus Meigen, 1818 ; † Culex mosquito Robineau-Desvoidy, 1827 ; † Culex frater Robineau-Desvoidy, 1827 ; † Culex taeniatus Wiedemann, 1828 ; * Culex sugens Wiedemann, 1828 ; * Culex kounoupi Brullé, 1833 ; † Culex toxorhynchus Macquart, 1838 a; * Culex annulitarsis Macquart, 1846 a; locality not known, Culex viridifrons Walker, 1848 ; † Culex excitans Walker, 1848 ; # Culex inexorabilis Walker, 1848 (could be aegypti or formosus ); † Culex exagitans Walker, 1856 a; + Culex insatiabilis Bigot, 1959 ; Australia, Culex bancrofti Skuse, 1889 ; * Culex elegans Ficalbi, 1890b ; India, Culex rossi Giles, 1899 ; Australia, Stegomyia fasciata var. queenslandensis ; Theobald, 1901a; † Stegomyia fasciata var. luciensis Theobald, 1901a ; # Stegomyia nigeria Theobald, 1901a (could be aegypti or formosus ); + Stegomyia lamberti Ventrillon, 1904 ; Canary Islands, Stegomyia calopus var. canariensis Pittaluga, 1905 ; Philippines, Stegomyia fasciata ssp. persistans Banks, 1906b ; Tenerife, Canary Islands, Culex anguste -alatus Becker, 1908; Tenerife, Canary Islands, Culex albopalposus Becker, 1908 ; Philippines, Duttonia alboannulis Ludlow, 1911b ; Australia, Mimeteomyia pulcherrima Taylor, 1919 ; # Stegomyia fasciata var. atritarsis Edwards, 1920 a.

Note. An explanation of the complex nomenclatural history of the nominotypical subspecies is beyond the scope of this treatment. In summary, in the interests of nomenclatural stability, Mattingly et al. (1962) petitioned the International Commission on Zoological Nomenclature (ICZN) to fix the name Aedes (Stegomyia) aegypti ( Linnaeus, 1762) with designation of a neotype from Kuala Lumpur, Selangor, Malaya [ Malaysia]. The petition was validated in ICZN Opinion 711 (International Commission on Zoological Nomenclature 1964). See Clements & Harbach (2018) for an alternative perspective. Since we now know that the nominotypical form is an invasive species that was restricted to sub-Saharan Africa until only about 500 years ago, we think that the choice of Malaysia for the neotype and type locality, with an even more recent history of invasion than the initial movement to the New World, is problematic.