Acta Tropica 191 (2019) 162–171

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Microevolution of medically important mosquitoes – A review T

a,b,⁎
Lincoln Suesdek
a
Instituto Butantan, Av. Vital Brazil 1500, São Paulo, SP, CEP 05503-900, Brazil
b
Instituto de Medicina Tropical, Universidade de São Paulo, Av. Dr. Enéas de Carvalho Aguiar 470, São Paulo, SP, CEP 05403-000, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: This review intends to discuss central issues regarding the microevolution of mosquito (Culicidae) vectors of
Culicidae several pathogens and how this process impacts vector biology, disease transmission, and vector control at-
Vector-borne diseases tempts. On the microevolutionary context, it comparatively discusses the current knowledge on the population
Evolution genetics of representatives of the genera Aedes, Anopheles and Culex, and comments on insecticide resistance of
Adaptation
culicids. It also discusses other biological aspects of culicids that are not usually addressed in microevolutionary
Evolvability
studies, such as vectorial competence, endosymbiosis, and wing morphology. One conclusion is that mosquitoes
are highly genetically variable, adaptable, fast evolving, and have versatile vectorial competence. Unveiling
microevolutionary patterns is fundamental for the design and maintenance of all control programs. Sampling
methods for assessing microevolution must be standardized and must follow meaningful guidelines, such as
those of “landscape genetics”. A good understanding of microevolution requires more than a collection of case
studies on population genetics and resistance. Future research could deal not only with the microevolution sensu
stricto, but also with evolutionarily meaningful issues, such as inheritable characters, epigenetics, physiological
cost-free plasticity, vector immunity, symbiosis, pathogen-mosquito co-evolution and environmental variables. A
genotyping panel for seeking adaptive phenotypes as part of the standardization of population genetics methods
is proposed. The investigative paradigm should not only be retrospective but also prospective, despite the un-
predictability of evolution. If we integrate all suggestions to tackle mosquito evolution, a global revolution to
counter vector-borne diseases can be provoked.

1. Introduction
This review intends to discuss central issues on the microevolution
(evolution of populations within a species) of mosquitoes (Culicidae)
vectors of several pathogens and how this process impacts vector
biology and epidemiology. The present work is neither a complete re-
view of state-of-the-art microevolutionary studies, nor is the result of an
exhaustive literature search; however, it provides a critical opinion on
some key facts.
This theme has been repeatedly addressed in scientific and technical
literature, but in general it is mostly covered by independent case
studies of population genetics which are mostly atemporal and not
connected with other academic approaches. Moreover, many biological
traits, which may be raw materials for the microevolution of culicids,
such as plasticity, morphology, heritability, host-parasite interaction
and endosymbiosis, have been underrepresented or sometimes under-
estimated in this context.
The next sections present comparative discussions of traditional
points such as current knowledge on population genetics of
representatives of the genera Aedes, Anopheles and Culex and compare
them when feasible. To illustrate how microevolution occurs in
Culicidae, typical examples, such as cases of genetic population struc-
ture and development of insecticide resistance are addressed.
There are also comments on other biological aspects of culicids not
usually addressed in microevolutionary studies, such as vectorial
competence, endosymbiosis, and wing morphology. The inclusion of
these alternative biological characters is justified by the fact that many
of them are plastic, heritable or epigenetic, such that they cannot be
neglected in evolutionary approaches. Finally, as microevolution is an
obstacle to vector control and enhances disease spread, the impacts of
microevolution on vector control and epidemiology are here-
inconsidered.
The medical relevance and biological complexity of mosquitoes
justify the need for a permanent investigation into their microevolution.
Culicids are protagonists of the transmission of dozens of human and
animal pathogens including viruses, protozoans, worms and even tumor
cells (Benelli et al., 2016). Some diseases whose aetiological agents are
vectored by mosquitoes, such as Dengue and Malaria, affect hundreds

⁎
Corresponding author at: Instituto Butantan, Av. Vital Brazil 1500, São Paulo, SP, CEP 05503-900, Brazil.
E-mail address: lincoln.suesdek@butantan.gov.br.

https://doi.org/10.1016/j.actatropica.2018.12.013
Received 8 August 2018; Received in revised form 8 November 2018; Accepted 6 December 2018
Available online 07 December 2018
0001-706X/ © 2018 Elsevier B.V. All rights reserved.
L. Suesdek
of thousands of people worldwide and cause thousands of deaths anu-
ally. Severe morbidities are also frequent, as occurred in the Zika out-
break in the Americas (Cugola et al., 2016), when Zika viruses vectored
by Aedes aegypti (Linneaus) and Aedes albopictus (Skuse) caused mi-
crocephaly in thousands of newborns, a congenital syndrome char-
acterized by head underdevelopment.
As therapies and vaccines are not yet well stablished for most
mosquito-borne diseases, much effort must be focused towards mos-
quito control and surveillance. Vector control, in itself, is so challenging
that control programs have to be continuously reformulated and even
more comprehensive approaches have been proposed (Araujo et al.,
2015; Benelli and Beier, 2017). Hereafter, we discuss how our knowl-
edge of vector biology and control can benefit from deepening and
integrating microevolutionary studies.
2. Microevolution
Microevolution is a dynamic evolutionary process by which genetic
allele frequencies change under the taxonomic level of species (popu-
lations). The genetic events involved in microevolution include natural/
artificial selection, mutation, gene flow and genetic drift, being that the
process can lead to speciation and occur in short periods of time, in
contrast to macroevolution, above the level of species (reviews avail-
able in Mayr, 1942; Hendry and Kinnison, 2001).
A variety of empirical and experimental approaches can detect
microevolutionary patterns and processes. Static or dynamic observa-
tion of genotypes and phenotypes in populations, particularly popula-
tion genetics, often reveals the occurrence of microevolution. Even
macroevolutionary markers such as DNA barcoding may expose mi-
croevolutionary signals, as with the intraspecific divergence in the cy-
tochrome oxidase 1 gene of some species (Murugan et al., 2016;
Karthika et al., 2018).
From the human point of view, many mosquito species evolve ra-
pidly owing to the short generations, large numbers of offspring, high
mobility and high genetic variability. Evolution in some species may
occur within short periods, such that one can witness changes in in-
secticide tolerance, vectorial competence or reproductive behavior in
just a few years. Traits observed in culicids like anthropophily, do-
mestication and urbanization are also manifestations of microevolution.
Thus, when microevolution changes the way a mosquito reacts to the
environment, control actions may lose efficacy. In the cases, micro-
evolution becomes a barrier to vector control, which is important for
pathogens dispersal.
3. Population genetics
Population genetics is the main methodological approach to assess
central themes of microevolution, such as population structure, genetic
variability and phylogeography. This field has been extensively revised
in medically important culicids (Tabachnick, 1991; Urdaneta-Marquez
and Failloux, 2011). Based on the Web Of Science (2018) bibliographic
database, population genetics has been applied to mosquito evolution
investigations since as far as back the 1960s. Until nearly the 1990s, the
general approach towards this used to be characterizing karyotypes,
isoenzymes and random amplified polymorphic DNA of a few popula-
tions in small geographic areas. Between the years 1990–2010 s, more
geographically comprehensive studies were carried out using mi-
tochondrial, nuclear, and microsatellite DNA markers. More recently,
studies started focusing on addressing macrogeographic scales, using
more representative samples and panels of thousands of DNA single
nucleotide polymorphisms. Microgeographic studies are still being
carried out, taking the advantage of an extensive variety of genetic
markers to describe cases of locally restricted evolutionary patterns
(Simonato et al., 2016).
Hundreds of papers on the population genetics of Culicidae have
been published, but despite decades of accumulated knowledge and
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Acta Tropica 191 (2019) 162–171
methodological advancements, the geographical and ecological com-
prehensiveness of most studies are still insufficient to yield epidemio-
logically meaningful conclusions about populations of a given mosquito
species. Sampling has also been problematic as most authors hapha-
zardly choose populational samples, without observing methods vali-
dated for ecological sciences. Commonly, population structure patterns
are assigned to unequally sampled metapopulations from under-
represented biomes, which lead to biased or inconclusive findings.
Disappointingly, the field is still experiencing the Tower of Babel phe-
nomenon (Caterino et al., 2000), a lack of standardized markers, which
jeopardizes further comparisons, meta-analyses and generalistic inter-
pretations.
A possible solution to these problems would be to re-design these
studies using the ecological sampling guidelines recommended by the
“landscape genetics” (Manel et al., 2003) and other methods used in
Ecology (Kuno, 1991; Broquet and Petit, 2009). By linking formal cri-
teria for sampling with dispersion models based on the environment
and a robust population genetics, one would obtain more meaningful
epidemiology results. Population genetics studies, if conceived under
the light of Ecology and its comprising elements such as human activ-
ities, climate, and landscape physiognomy, can help estimate, for ex-
ample, the complete scenario of gene flow, the geographical extension
of a given genotype, the limits of metapopulations, where control
methods are more prone to fail, etc.
Population genetics has also been used to describe, explicate and
predict the spread of insecticide resistance genes, but this approach is
still tame. Neutral markers are often used for investigating micro-
evolution from the academic angle, but loci under selection such as
those with resistance alleles, should also be included because they may
be applied in vector control practices.
All the above-mentioned improvements must be accompanied by a
rigorous standardization of biological markers, as suggested by
Caterino et al. (2000), in an attempt to avoid the “Tower of Babel”
effect. In the particular case of medically-important culicids, genetic
markers for key phenotypes such as vectorial competence, resistance
and other evolvable features (discussed in the next sections) must be
gathered in a genotyping panel. Such panel should be employed in all
future studies to unveil microevolution that is really significant to
epidemiology.
The state-of-the-art of this field, composed of hundreds of available
papers denotes that the most studied Culicidae genera are Aedes,
Anopheles and Culex (Web Of Science, 2018) bibliographic database.
Accordingly, we comment on key evolutionary facts regarding these
three genera, with emphasis on some of the main pathogen-vector
species.
3.1. Aedes
The genus Aedes harbours some of the most relevant vector species
worldwide. One of them, Aedes aegypti, a vector of several for arbo-
viruses, is genetically rich either in absolute terms or in comparison to
other Culicidae species, as revised by Urdaneta-Marquez and Failloux
(2011). One of the most geographically comprehensive research papers
on Ae. aegypti (Gloria-Soria et al., 2016a) shows its enormous genetic
variability and the remarkable differentiation between its sylvatic (Ae.
aegypti. formosus) and domestic (Ae. aegypti aegypti) forms in Africa,
where the species presumably originated.
In areas where Ae. aegypti is exotic, namely Asia, Europe, and
Americas despite the genetic drifts and bottlenecks resultant from being
introduced, high levels of nucleotide richness and haplotype diversity
as well as multiple coexisting introduced lineages are commonly found
(Gorrochotegui-Escalante et al., 2002; Ayres et al., 2004; Bracco et al.,
2007). Population structure in exotic Ae. aegypti is usually found
(Urdaneta-Marquez and Failloux, 2011) and genetic diversity of this
species appears to be high even on a microgeographical scale (Ayres
et al., 2004). A usual interpretation is that the original variability of Ae.
L. Suesdek
aegypti in Africa is very high. This arguably supported the variability of
the exported exotic populations and it may be considered an example of
retention of polymorphism.
In the Americas, Ae. aegypti underwent a complex life history since
its earliest introductions in the XVI century. It was eradicated in several
countries by the middle of the XX century owing to a Pan-American
effort enhanced by DDT insecticide, but despite that success, re-in-
festation occurred just a few decades later probably by invasion from
neighboring areas (Kotsakiozi et al., 2017) or overseas (Bracco et al.,
2007). In addition to that turbulent population dynamics, particularly
in Brazil, the population genetics of this species have become even more
complex due to contemporary introductions from abroad via sea ports
(Bracco et al., 2007). These facts illustrate the resilience of this species
and its ability to invade and adapt fast.
Most commonly, genetic divergence in this species is not correlated
with geographical distance, and gene flow is geographically restricted,
although opposite cases are also found (Gorrochotegui-Escalante et al.,
2000, 2002). In contrast to its regionalized gene flow, Ae. aegypti is very
spreadable from the ecological standpoint, but important geographical
barriers such as wide water bodies may negatively impact its gene flow
(Vadivalagan et al., 2016).
It is also noteworthy that Ae. aegypti evolves fast. In fact, Ae. aegypti
has become anthropophilic, domestic and has rapidly colonized other
areas outside Africa in the last 4000 years, mostly influenced by human
activities (Powell and Tabachnick, 2013; Brown et al., 2014). The
successful spread and adaptation of Ae. aegypti in some cases have been
even faster, as genetic and behavioral changes occurred within a few
decades (Brown et al., 2014; Gloria-Soria et al., 2016a, b). The con-
generic Ae. albopictus is also genetic rich, invasive, and adaptable (Chen
et al., 2015)
3.2. Anopheles
Remarkably, this genus of exclusive vectors of human malaria has
cases of species complexes undergoing incipient speciation, partial re-
productive isolation and introgression (Powell et al., 1999; Walton
et al., 2001; Moreno et al., 2007), which enormously contribute to
genetic variability and microevolution. The most prominent complex is
Anopheles gambiae s.l.
Population genetics of representatives of the genus Anopheles has
been broadly investigated, and species generally present great diversity,
as exemplified by several research papers (Walton et al., 2001; Pinto
et al., 2002; Kayondo et al., 2005; Oshaghi et al., 2007; Poolprasert
et al., 2008; Brochero et al., 2010; Deitz et al., 2012; Sarma et al., 2012;
Markianos et al., 2016) and documented in reviews (Manguin et al.,
2008; Loaiza et al., 2012). Anopheles gambiae s.s. Giles is perhaps the
most genetically polymorphic species hitherto known; individuals may
bear 1.7–2.7 million variant alleles, as reported by a comprehensive
research paper (Miles et al., 2017).
The main Anopheles species have not migrated across biogeo-
graphical regions as some species of Aedes and Culex have, rather, their
diversification is more local. One exception to this was the transient
establishment of Anopheles gambiae s.l. in Brazil during the 1930s,
which was later eradicated (Tauil et al., 1985; Levine et al., 2004).
These peculiarities of this genus are also manifested in other bio-
geographical regions. Anopheles species with differential vectorial ca-
pacities among populations or comprising cryptic genetic taxa have
been widely detected in Asia (Sinka et al., 2011). In South America,
cryptic species are present (Loaiza et al., 2012) and the broad dis-
tribution of Anopheles darlingi is marked by highly structured popula-
tions in Amazonia (Campos et al., 2017a).
Environmental variables such as geographic distance, barriers and
landscape continuity are decisive in shaping the genetic population
structure of An. gambiae s.l (Walton et al., 2000; Miles et al., 2017).
Human activity is also recognized to impact microevolution of this
species (Costantini et al., 1999; Miles et al., 2017). These facts reinforce
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our already mentioned suggestion of landscape genetics for deciphering
microevolution of Anopheles in the epidemiological context.
Concerning microevolutionary rates and times, several disruptive
and stabilizing events have been estimated to have occurred in the
Anopheles genus in the Pleistocene (Matthews et al., 2007; Mirabello
and Conn, 2008; Scarpassa and Conn, 2011), but contemporary and
seasonal haplotypic fluctuations were also reported (Angella et al.,
2007).
3.3. Culex
This genus also has taxonomic complexes. The most prominent is
the Culex pipiens Assemblage (sensu Harbach, 2012), which comprises
Cx. pipiens Linneaus, Cx. quinquefasciatus Say, Cx. molestus Forskål, Cx.
pallens Coquilett and Cx. australicus Dobrotworsky & Drummond, also
vectors of several pathogens. The assemblage might be even more
complex as it may contain other uncharacterized taxa (Cornel et al.,
2012; Dumas et al., 2016).
Hybrid zones between representatives of the Cx. pipiens Assemblage
occur in North America (Fonseca et al., 2004; Kent et al., 2007), South
America (Humeres et al., 1998; Farajollahi et al., 2011; Carvalho et al.,
2017), Africa (Farajollahi et al., 2011; Shaikevich et al., 2016), Europe
(Becker et al., 2012; Osorio et al., 2014), Middle East (Harbach, 2012),
Eastern Asia (Shaikevich et al., 2016), and Australia (Farajollahi et al.,
2011). Introgression does not happen in all hybrid zones, but when
present, it influences microevolution as it combines genes and produces
diversity. In Europe, introgression between Cx. molestus and Cx. pipiens
yield novelties on biting behavior (Ciota et al., 2013) and between Cx.
pipiens and Cx. quinquefasciatus (Shaikevich et al., 2016), diverse gen-
otypes. In Asia, there is documented introgression between Cx. pallens
and Cx. quinquefasciatus (Fonseca et al., 2009). The introgression in-
volving Cx. pipiens and Cx. quinquefasciatus is especially problematic
because hybrids may combine the human-biter behavior of Cx. quin-
quefasciatus with the vectorial competence to the West Nile virus of Cx.
pipiens, and enhance the spread of this pathogen in North America
(Fonseca et al., 2004; Ciota et al., 2013; Brugman et al., 2018).
Many research articles discuss the genetic variability of re-
presentatives of the Cx. pipiens Assemblage, but there is a lack of meta-
analyses and reviews. This, added to the complexity of the Assemblage,
make it difficult to describe a global scenario of population genetics for
that taxa. Another issue is that studies use several different genetic
markers with distinct evolutionary rates, such as mitochondrial and
nuclear DNA (Toews and Brelsford, 2012). In some cases, sampling
sizes, genetic and geographical representativity are unstandardized and
variable making it difficult to compare studies.
A global study of Culex quinquefasciatus revealed that Asian and East
African populations have higher allelic richness than populations from
the Americas, West Africa and other parts of the word (Fonseca et al.,
2006). Presumably, the origin of this cosmopolite species is East Africa
(Harbach, 2012), but populations from other biogeographic regions
were introduced, which somehow resembles the case of Ae. aegypti.
However, gene flow is usually geographically broader in Cx. quinque-
fasciatus (Lõhmus et al., 2012; Morais et al., 2012).
Low genetic variability of Cx. quinquefasciatus was reported in
several places worldwide, (Pfeiler et al., 2013; Ashfaq et al., 2014; Low
et al., 2014; Werblow et al., 2014; Vadivalagan et al., 2017), but cases
of higher levels of mitochondrial diversity also exist (Sharma et al.,
2010). On the other hand, Culex pipiens from the Po river delta
(southern Europe), a place with insecticide-free natural habitats, pre-
sented higher genetic diversity and population variability (Simonato
et al., 2016).
4. Insecticide resistance
Resistance to xenobiotics is probably the most eloquent and docu-
mented example of rapid microevolution in Culicidae (Hemingway and
L. Suesdek
Ranson, 2000; Srivastava et al., 2010; Liu, 2015). Mosquitoes have
notably developed resistance to many insecticides during the last dec-
ades, which is a really short period in evolutionary terms. Heritability
and resistance mechanisms have been investigated for decades (Liu,
2015) and currently, several genes present in the maintaxa (Aedes,
Anopheles and Culex) are enough for detoxifying several insecticides
(Coetzee and Koekemoer, 2013; Nkya et al., 2014; Moyes et al., 2017;
Ingham et al., 2018).
This phenomenon is also a clear example of how human behavior
alters mosquito evolution (Failloux and Rodhain, 1999). Studies of the
spread and stability of resistance genes show that the presence of the
insecticide (selective pressure) is usually a sine qua non condition for
maintening of resistance (Liu, 2015). Thus, as natural selection acts on
these genes, the inclusion of genetic markers that encompass them is
strongly recommended in microevolutionary studies. In principle, as
mosquitoes can evolutionarily increase their refractoriness to in-
secticides, they can overcome other control methods, co-evolve with
pathogens, and adapt to rapid environmental changes. In fact, most of
these processes have already been seen in nature.
Resistance severely impacts microevolution, vector control, and
epidemiology. The need for an accumulative listing of resistance genes
is already recognized (Donnelly et al., 2016). It is strongly re-
commended that specialists in this field update shareable repositories of
resistance genes (Moyes et al., 2017). These databases should be fed
with quantitative and qualitative information on alleles (as those de-
scribed by Weetman et al., 2010) and linked to a genotyping panel for
investigating population genetics and microevolution.
5. Domestication and adaptation
In Culicidae, domestication, and more importantly, urbanization,
are conspicuous results of microevolution. Cases of domestication, ur-
banization and anthropophily are frequent (Costantini et al., 1999;
Multini et al., 2016; Medeiros-Sousa et al., 2017; Shragai et al., 2017)
and natural selection of genes correlated to domestication have been
reported.
It is reasonable to think that domestication is a pre-adaptation
(sensu Ridley, 2004) of the anthropophilic Ae. aegypti and Cx. quin-
queafsciatus, some of the few species capable of living in the most ur-
banized metropoles. The urban environment is dramatically different
from nature. It has several constraints and selective pressures which
were not present when the early diversification events of these species
took place (> 1 mya). The genetic richness of these species might allow
them to rapidly adapt to contemporary habitats.
Knowledge on the genetic bases of domestication in culicids is still
arid, which opens an important scientific field. It is uncertain why some
species can develop in anthropic habitats whereas others can not. A
good hypothesis to be investigated in this field is that more diverse
species are more prone to adapt to domestic habitats. However, this
issue appears to be more complex when we compare some neotropical
species. There are cases of highly variable species that became do-
mesticated recently, such as Aedes scapularis Rondani (Petersen et al.,
2015), whereas others remained sylvatic despite their genetic richness,
as seen in Anopheles cruzii Dyar and Knab (Lorenz et al., 2014).
Natural selection, adaptation, and other elements may be involved
in the evolution of domestication observed in culicids. As advocated by
Reznick and Ghalambor (2001), when an invasive species colonizes a
new environment with new food sources, habitat, and predators, it is
subjected to new selective pressures and may evolve rapidly. Yet ac-
cording to those authors, rapid adaptive evolution may also take place
in populations with complex genetic structures living in their original
heterogeneous environments. Rapid evolution are exemplified by cases
where habitats were disturbed by anthropic activity.
In this context, maybe the finest question to be answered would be
what gene allelles confer adaptability for “living among humans”.
Differently from the usual genetic markers for evolution, such alleles
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Acta Tropica 191 (2019) 162–171
are not selectively neutral, but they should be unveiled and included in
a genotyping panel for tracking adaptation to human habitats.
6. Genetic control of vectors
In a simplistic view, if genetic control of mosquitoes is about
cheating evolution (Champer et al., 2016), their natural microevolution
is a limiting factor to this method (Alphey, 2014). Genetic control
methods in a broad sense, such as Incompatible Insect Technique (IIT),
Sterile Insect Technique (SIT), Release of Insects carrying a Dominant
Lethal (RIDL), etc., are not microevolution-proof and are, thus, con-
stantly subjected to resistance (Alphey, 2014; Leftwich et al., 2016).
Indeed, many authors agree that the population genetics of the target
species for genetic control should first be finely assessed (Alphey, 2014;
Gloria-Soria et al., 2016a).
Genetic-based demographic estimates such as effective population
size, gene flow and number of migrants are mandatory parameters to be
known before, during and after applying a genetic control action, as the
effectiveness and/or spread of the released genetic trait will directly
depend on them (Gloria-Soria et al., 2016a; Saarman et al., 2017).
Notedly, they show discrepancies when contrasted to non-genetic de-
mographic estimates, which sometimes makes them difficult to apply in
practice. In spite of its limitations, genetic population parameters are
not dispensable in mosquito demographics because they provide a
useful notion of major genetic effects, breeding structure and re-
production mode of a population prior to or poster to any control
program be applied (Pinto et al., 2002; Athrey et al., 2012; Saarman
et al., 2017; Pierson et al., 2018). All of these parameters should be
accomplished in a temporal perspective. In general terms, current
considerations also apply to issues mentioned in the section “Wolba-
chia”.
Another concern to be considered is how genetic control may alter
microevolution of mosquitoes. Especially in cases of population sub-
stitution, when genes of interest are inserted in a natural population,
there is no a definitive prediction of how the novel genes will impact
subsequent microevolution of the targeted population. Theoretically,
since many genes are epistatic, the possibility of a negative impact
cannot be ruled out. Even in cases of population suppression, as no
strategy is immune to evolution, it is very important to estimate if the
pressure of lethal genes can drive natural populations in an unwanted
evolutionary direction. Mathematical models, empirical studies, field
and semi-field may help cover these concerns. Safety of genetic control
has been carefully discussed (Carballar-Lejarazu and James, 2017).
7. Vector-pathogen coevolution
Vector-pathogen interactions encompass classic cases of coevolu-
tion. Bearing in mind that in this co-evolutionary system, vectors are in
fact hosts, many interpretations resulting from host-parasite ecology are
valid for this discussion.
Resistance to pathogens has adaptive value for mosquitoes, but
pathogens in turn, also suffer selection and may adapt to vectors
(Hansen and Koella, 2003; Barillas-Mury and Kumar, 2005). This kind
of co-evolution usually tends to reach reciprocal survival status by
means of finely equilibrating virulence, tolerance, and resistance
(Cohuet et al., 2010). This complex evolutionary balance has been
studied in practice (Cohuet et al., 2010) and in theory (Gandon and
Michalakis, 2002; Restif and Koella, 2004), and although this theme is
far from being satisfactorily understood, it is largely accepted that
viruses, protozoans, and worms may affect mosquitoes´ microevolution
(Cohuet et al., 2010).
Intuitive thinking could lead to the belief that the relevance of pa-
thogens to the microevolution of insect vectors is marginal. Prevalence
of most pathogens in mosquitoes is low, as observed in Dengue, Zika,
Yellow fever, Plasmodium, etc., such that it is difficult to conceive how
just a few infected individuals can affect the evolution of such
L. Suesdek
demographically rich insects.
However, several models and cases demonstrate that even low
prevalent parasites can shape host evolution, mainly in instances where
the ecological host-parasite association are recent (May and Anderson,
1979). According to those authors, the equilibrium between resistance
and tolerance of insects to a new pathogen takes some time to develop.
During that period, the species is more sensitive to pathogen-driven
selection. This theory raises concerns about the recent introduction of
Zika virus in South America, considering the promotion promotion of
new ecological interactions with Ae. aegypti, humans, sylvatic primates
and maybe sylvatic mosquitoes (Terzian et al., 2018). This new scenario
may culminate in rapid mosquito microevolution and the consequences
can be dramatic. Hence, studies integrating genetics, ecology and epi-
demiology are urgent in this case.
Vectorial competence is widely spread in the family Culicidae and
many species share competence to the same pathogens. It would be a
significant contribution to knowledge if all the genetic determinants for
vectorial competence were identified. Genetic vector control could
benefit from this finding by designing antagonistic “gene drive” solu-
tions with a broad phylogenetic spectrum.
The fact that vectorial competence is partly genetically determined
(Fansiri et al., 2013; Juneja et al., 2015; Souza-Neto et al., 2019) is a
reason to include it in the list of central elements of mosquito micro-
evolution. Similarly, vector capacity traits and other heritable char-
acters related to host-vector or vector-pathogen interactions should be
considered as raw materials for microevolution. One may cite mosquito
immunity and chemosensory genes as examples (Neafsey et al., 2015).
8. Wing shape
Wing shape in Culicidae is a complex character apparently de-
termined by polygenic inheritance and it is species-specific (Dujardin,
2008; Lorenz et al., 2017). The wing outline is probably constrained by
canalization, but the internal relative positions of the wing veins may
be selectively neutral (Dujardin, 2008; Lorenz et al., 2017). Theoreti-
cally, wings are good models for studying microevolution, and in
practice, many examples confirm that.
In the neotropical Anopheles darlingi Root (Motoki et al., 2012) and
Ae. aegypti (Vidal and Suesdek, 2012), wing shape revealed population
structure, although the distances between intraspecific populations do
not correlate to their genetic distances. Microgeographic population
structure can also be assessed using wing shape, as observed in Culex
nigripalpus Theobald (Carvalho et al., 2017) and Anopheles cruzii
(Lorenz et al., 2014).
Morphometric evaluation of wing shape during short periods
showed that 4 years (Vidal et al., 2012) and 14 months (Louise et al.,
2015) were sufficient for Ae. albopictus and Ae. aegypti (respectively) to
accumulate wing shape changes. In the case of Ae. aegypti (Louise et al.,
2015), microsatellite DNA variation accompanied wing microevolution
during the same interim.
Thus, many evidences point to the fact that wings are indicators of
microevolution in Culicidae. Although most quantitative parameters
obtained from genetics cannot be retrieved from wings (Dujardin,
2008), morphometric description of wing shape is cheap and can serve
as a preliminary assessment of evolutionary patterns (Dujardin, 2008;
Lorenz et al., 2017).
A recent achievement of geometric morphometrics (Petersen et al.,
2015) permits one to quantify the morphological diversity (MD) of a
given population, which is partially correlated to genetic variability.
We are still investigating aspects of this correlation, but currently, it is
already possible to detect populations with high MD and presumably
with high genetic diversity. Considering that the genetic richness of
Culicidae is indicative of and proportional to epidemiological relevance
(Gloria-Soria, et al 2016a), MD is a useful estimator of potential nox-
iousness. Technically, the computation of MD is relatively simple
(Petersen et al., 2015) and as cheap as other morphometrical
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Acta Tropica 191 (2019) 162–171
Fig. 1. Graphical representation of a morphospace of two principal components
of the wing shape of Aedes aegypti. Shape coordinates were extracted from the
geometrical positions of 18 wing landmarks (as defined by Petersen et al.,
2015). Populational samples (with 10 individuals each) H and L showed high
and low dispersal of individuals in the plot, which means high and low mor-
phological diversities, respectivelly. The genetic variability (not shown) of H is
consistently higher than that of L. This simplistic example illustrates the partial
correlation between morphological and genetic markers.
estimators. The usual outcome of this estimator and its interpretation
are depicted in Fig. 1.
Owing to the informativeness and rapid evolution of wings, re-
positories of wing data have been encouraged (Dujardin et al., 2010).
The recently launched WingBank (Lorenz et al., 2017), a database of
∼14,000 wing pictures, aims to document wing shape worldwide over
time and to provide a connection between scientists and non-academic
health professionals for identifying mosquito populations and species.
The next developmental step of WingBank should be to incorporate an
automated system for the identification of samples (i.e. individuals,
populations, species).
9. Wolbachia
These endosymbiotic bacteria manipulate the reproduction and
physiology of mosquitoes, and can alter host evolution (Werren et al.,
2008). Wolbachia may have a central role in insect speciation
(Bordenstein et al., 2001), as reported in Cx. pipiens from South Africa
(Dumas et al., 2016) and Cx. pipiens pallens in China (Chen et al., 2013).
The population genetics parameters can be altered by the presence
of Wolbachia. By natural means, variability of mitochondrial DNA may
be diminished in Wolbachia-infected mosquitoes (Rasgon et al., 2006;
Morais et al., 2012). Lateral gene transfer between Wolbachia and
mosquitoes are also a source of genetic novelties.
Owing to its potential to interfere in the host´s general biology,
Wolbachia has been used as a tool to reduce vectorial competence in
mosquitoes. Artificially-infected lineages of Ae. aegypti have been re-
leased in-field, introducing new phenotypes and successfully changing
the genetic background of natural mosquito populations (Fraser et al.,
2017; Flores and O’Neill, 2018).
The fact that Wolbachia has been used to control mosquitoes via
population substitution, suggests that this method is an artificial mi-
croevolutionary process. All mentioned information reinforce the idea
that one has to be familiar with the population genetics of target species
in Wolbachia-mediated control. Analogous to the suggestions of the
section “genetic control of vectors”, the use of Wolbachia in driving
populational substitution would profit from accompanying estimates of
the possible impacts of this intervention on natural microevolution.
Evolutionary outcomes and safety of Wolbachia-mediated control have
been actively debated (Popovici et al., 2010; Bull and Turelli, 2013;
Caragata et al., 2016; King et al., 2018).
L. Suesdek
10. Other polymorphic phenotypes
Many physiological, behavioral and reproductive traits are variable
and inherited, which confers evolutionary significance on them.
Variable inherited characters may be subjected to natural selection and
their genes may suffer mutation, genetic drift, and other evolutionary
forces. Mosquitoes present several traits under those conditions such
that they constitute raw materials for the microevolution of these in-
sects.
One may include in this category, transovarial pathogen transmis-
sion (Bosio et al.,1992; Ferreira-de-Lima and Lima-Camara, 2018), ve-
neran virus transference (Campos et al., 2017b), anthropophily,
odorant preference of Ae. aegypti for humans (McBride et al., 2014), and
autogeny in Culex pipiens (Becker et al., 2012). Morphological variation
as reported in Anopheles (Lehmann and Diabate, 2008) and Aedes
(Powell and Tabachnick, 2013) also can account for microevolution.
Regarding behavior, it is widely known that many urban mosquito
species exhibit a disruptive flight when trying to escape from human
slaps. According to my memories from childhood (∼30 years ago in
Brazil), it used to be easier for us to hunt and kill Ae. aegypti. This
hypothesis, if correct, would be an example of rapid evolution of a
human-driven mosquito behavioral trait.
It is necessary to encourage investigation on the evolvability of
plastic and epigenetic characters of mosquitoes. It is well known that
epigenetic features, such as DNA methylation and other post-transla-
tional modifications may be inherited, despite their non-genic nature
(Vilcinskas, 2017). Epigenetic characters significantly account for
phenotypic plasticity and adaptability and this manifestation can be
more rapid and effective than natural selection (Trerotola et al., 2015).
Thus, if this phenomenon lead to adaptation in Culicids, it would be
particularly worrying and should be further studied. Expressive datasets
on mosquito epigenomics are already available and may serve as a good
starting point for such research (Gomez-Diaz et al., 2014).
Apart from the already known evolvable characters of culicids, it is
paramount to drive efforts to discover quantitative trait loci (QTLs)
responsible for any phenotype that influence the epidemiology of
mosquito-borne diseases. A way to achieve this could be the estab-
lishment of a consortium of scientists dedicated to finding and vali-
dating QTLs. Once found, such QTLs could be included in genotyping
panels for applied microevolutionary studies.
In principle, any biological trait which could at least minimally
interfere in mosquitoe evolution, directly or indirectly, is worth re-
searching owing to the complexity of the all mosquito-borne disease-
related question. All those characters should be included in future po-
pulation genetic studies because the possibility of evolution involves
them, and may significantly impact on vector biology, and in turn,
epidemiology.
11. Conclusions
An impressive quantity of data is available concerning the micro-
evolution of Culiclidae mosquitoes, which leads us to make several
conclusions and pose new hypotheses. On the other hand, it is clear that
at this moment a significant portion of the results and observations
cannot be meta-analyzed owing to the lack of standardization of the
methods.
In a simple comparison of population genetics data among the three
most studied taxa, Aedes aegypti, Anopheles gambiae s.l. and Culex pipiens
Assemblage, one can identify several similarities. All of them present
genetic richness, variability, and polymorphism, especially Ae. aegypti
(Gloria-Soria et al., 2016a) and An. gambiae s.s. (Miles et al., 2017).
Despite successive genetic bottleneck events suffered by exotic popu-
lations of Ae. aegypti, its polymorphism remained high in several cases
(Urdaneta-Marquez and Failloux, 2011). A smaller number of com-
prehensive surveys and review papers have been dedicated to the Culex
pipiens Assemblage, but it appears to be also variable, although cases of
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Acta Tropica 191 (2019) 162–171
relatively low variability have been reported (Ashfaq et al., 2014; Low
et al., 2014; Pfeiler et al., 2013; Werblow et al., 2014). The list of
common features is even longer. Hybridization, introgression and in-
complete reproductive isolation between closely related species occur
and represent a source of genetic novelties in those three main taxa.
Other evolutionary meaningful aspects such as domestication, adapta-
tion to recently-altered habitats, competence to multiple pathogens and
insecticide resistance are also shared by many representatives of the
genera, Aedes, Anopheles and Culex.
Differences among them can also be identified. Ae. aegypti has a
peculiar capacity to live in dry places with scarce water sources, Cx.
quinquefasciatus can breed in highly polluted water and autogeny is
restricted to some populations (of Cx. pipiens, for instance). The species,
Ae. aegypti, Aedes albopictus, Culex pipiens and Culex quinquefasciatus are
invasive, urban and nearly cosmopolite whereas, Anopheles sp. has been
more prone to remaining in their original biogeographic region.
However, human activity has strongly influenced microevolution of all
of these species.
This genetic variability of culicids confers on the species a great
evolutionary potential, which is compatible with the remarkable
adaptability of the species. By analogy, the evolutionary features shared
by these species may help us understand the less known taxa.
The microevolutionary patterns are fundamental for designing and
maintening all control methods. For instance, this knowledge is a key
factor for deciding between using small-area interventions to control
highly structured populations of Anopheles darlingi in Amazonia
(Campos et al., 2017a) or using a broader action to mitigate a less ge-
netically variable population of Culex quinquefasciatus in Mexico
(Pfeiler et al., 2013). Moreover, these patterns may be explicative for
pathogen spread, as seen in the population structure of Culex tarsalis
Coquilett, which is congruent West Nile virus dispersion in North
America (Venkatesan and Rasgon, 2010).
Regarding the evolutionary velocity, one can state that mosquitoes
evolve rapidly relatively to human standards. This is worrying, but on
the other hand, this is an opportunity for scientists to witness and in-
vestigate this phenomenon within a human lifetime. Several examples
of rapid evolution were evidenced by neutral genetic markers (Gimnig
et al., 1999; Nayar et al., 2002, 2003; Campos et al., 2012; Louise et al.,
2015), adaptive resistance genes (Srivastava et al., 2010; Guidez et al.,
2017) and complex phenotypes (Vidal et al., 2012; Louise et al., 2015).
Even when the geographic signal is strong for population structure,
temporal variation can be detected, as reported for Ae. aegypti (Gloria-
Soria et al., 2016a). The velocity of microevolution in mosquitoes is
noticeably forged by a set of elements, including: short generations,
environmental dynamism and selective pressures imposed by humans,
pathogens and endosymbionts.
Taking data together, we conclude that mosquitoes are highly ge-
netically variable, adaptable, fast-evolving and have versatile vectorial
competence, which puts them amongst the most harmful living beings.
Without adequate investigation of their evolution, the current public
health scenario of “chronic” epidemics (such as malaria in Africa) or
sudden outbreaks (like Zika and yellow fever in South America) may
become unaltered or even worse.
Although numerous, most papers on microevolution of mosquitoes
are not interconnected so one cannot properly establish comparisons
among geographic areas and populations of the studied species.
Similarly, local patterns, rather than broad processes, are preferentially
addressed and the lack of temporal continuity of most studies jeo-
pardizes the recognition of evolutionary trends.
Scientists could take advantage of the rapid microevolution of
mosquitoes to investigate processes in real time. For instance, a tem-
porally continuous survey of cohorts may facilitate the evaluation of the
dispersal rate of mutations, artificial genes and parasites. Hence, the
investigative paradigm would not be only retrospective but also pro-
spective, despite the unpredictability of evolution. Also, since, vaccines
and remedies cannot be developed fast enough to mitigate vector-borne
L. Suesdek
diseases, more emphasis should be laid on mosquito evolution.
12. Perspectives
In the near future, research could deal not only with microevolution
sensu stricto, but also with other evolutionarily meaningful issues, such
as inheritable characters, epigenetics, physiological cost-free plasticity,
vector immunity, symbiosis, pathogen-mosquito coevolution, and en-
vironmental variables. The assembly of a genotyping panel comprising
evolvable traits that are significant to epidemiology has been re-
commended in many sections of this paper. This panel must include
genes encoding resistance, tolerance to pathogens, vector competence,
and anthropophily and should initially be used to obtain a genotypic
baseline of parameters (allele frequency, diversity, heterozigosity, gene
flow, etc.) of relevant mosquito populations, from which explanatory
and predictive studies can be drawn. Subsequently, this panel should be
included in all future studies as a gold standard to track the noxiousness
of any species in light of microevolution. Concominantly, sampling
methods must be standardized and should follow meaningful guide-
lines, such as those of “landscape genetics” (Manel et al., 2003).
As a mid-term strategy, all data derived from genotyping should be
input in existing or new databanks to facilitate the connection of
eclectic information. The appropriate softwares can then process data,
identify hotspots, rank priorities and help make decisions regarding
vector control or other initiatives. A promising, but not exclusive way to
do that would be to align mosquito vector data with the One Health
program (an integrative multi-sectorial strategy to improve public
health), as proposed by Benelli and Duggan (2018). Analogous to what
is being expected from the “personalized medicine” (Offit, 2011), the
computational processing of microevolutionary information would
make the creation of a customized and species-specific vectorial control
viable.
A good understanding of microevolution requires more than a col-
lection of study cases on population genetics and resistance. It can be
assumed that our microevolution investigation skills are developed
enough to support more integrated actions and studies involving in-
secticides, repellents, epidemics, vector control, dispersal, and phy-
siology. Suggestions are summarized in Fig. 2.
The scientific community has the expertise to deal with multi-
disciplinary projects and the current computational developments al-
lows us to cope with big data. With such potential installed we can
develop, in an orchestrated way, explicative and predictive mathema-
tical-statistical models incorporatingcomprising all that it is known
168
Acta Tropica 191 (2019) 162–171
Fig. 2. Summarized suggestions for
mosquito control to cope with mos-
quito microevolution better.
Traditional biological markers should
be combined with heritable and evol-
vable non-traditional characters in
order to investigate microevolution.
The whole data set should be as-
sembled in standardized databanks.
From this point on, mathematical and
statistical models should be applied to
permit a holistic interpretation of data.
This should be followed by enhancing
our understanding of the past and the
possible future scenarios of mosquito
evolution and, thus, the epidemiology
of vector-borne diseases.
about noxious mosquitoes. If we integrate all these suggestions for
tackling mosquito evolution, a revolution can be provoked for coun-
tering vector-borne diseases at a global scale.
Conflict of interest
I declare no competing interests.
Funding
Grants were received from Fundação de Amparo à Pesquisa do
Estado de São Paulo #2006/02622-5, #2014/27172-9 and #2016/
50008-6, from Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior, 23038.005.274/2011-24 and from Conselho Nacional de
Desenvolvimento Científico e Tecnológico #311805/2014-0.
Acknowledgements
I thank André Wilke and the three anonymous reviewers for critical
reading of the manuscript.
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