See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/272083419
Environmental and Genetic Factors Determine Whether the Mosquito Aedes
aegypti Lays Eggs Without a Blood Meal
Article  in  The American journal of tropical medicine and hygiene · February 2015
DOI: 10.4269/ajtmh.14-0471 · Source: PubMed
CITATIONS READS
2 70
6 authors, including:
Cristina Ariani Jewelna Osei-Poku
Wellcome Sanger Institute Noguchi Memorial Institute for Medical Research
27 PUBLICATIONS   305 CITATIONS    27 PUBLICATIONS   272 CITATIONS   
SEE PROFILE SEE PROFILE
Punita Juneja
University of Cambridge
38 PUBLICATIONS   316 CITATIONS   
SEE PROFILE
Some of the authors of this publication are also working on these related projects:
The role of dominant midgut bacteria isolated from Anopheles mosquitoes in Ghana in larval development and susceptibility to Plasmodium infection. View project
All content following this page was uploaded by Jewelna Osei-Poku on 16 June 2015.
The user has requested enhancement of the downloaded file.
Am. J. Trop. Med. Hyg., 92(4), 2015, pp. 715–721
doi:10.4269/ajtmh.14-0471
Copyright © 2015 by The American Society of Tropical Medicine and Hygiene
Environmental and Genetic Factors Determine Whether the Mosquito Aedes aegypti Lays Eggs
without a Blood Meal
Cristina V. Ariani,* Sophia C. L. Smith, Jewelna Osei-Poku, Katherine Short, Punita Juneja, and Francis M. Jiggins
Department of Genetics, University of Cambridge, Cambridge, United Kingdom
Abstract. Some mosquito strains or species are able to lay eggs without taking a blood meal, a trait named autogeny.
This may allow populations to persist through times or places where vertebrate hosts are scarce. Autogenous egg
production is highly dependent on the environment in some species, but the ideal conditions for its expression in
Aedes aegypti mosquitoes are unknown. We found that 3.2% of females in a population of Ae. aegypti from Kenya
were autogenous. Autogeny was strongly influenced by temperature, with many more eggs laid at 28°C compared
with 22°C. Good nutrition in larval stages and feeding on higher concentrations of sugar solution during the adult
stage both result in more autogenous eggs being produced. The trait also has a genetic basis, as not all Ae. aegypti
genotypes can lay autogenously. We conclude that Ae. aegypti requires a favorable environment and a suitable genotype
to be able to lay eggs without a blood meal.
INTRODUCTION been reported in Ae. aegypti populations from East Africa,
with the highest frequency (34%) recorded in Uganda.18
Approximately 14,000 species of insects have evolved to
1 The autogeny trait is highly environmentally dependent infeed on blood, and 300–400 of these species pose a threat other species,19–21 however the ideal conditions for its expres-
to humans.2 The blood-feeding insects depend on blood in sion in Ae. aegypti mosquitoes are unknown. In this study,
different manners. There are some species, such as the floor we investigated the factors that can influence autogeny in
maggot, Auchmeromyia luteola, that only feed on blood Ae. aegypti. We found that temperature and nutrition during
during the larval stage3; other species feed exclusively on larval and adult stages are the main environmental factors
blood throughout their life cycle, such as tsetse flies and affecting the expression of autogeny. Furthermore, there is
triatomine bugs,4,5 and a third group relies upon a blood genetic variation in the trait as different mosquito lines differ
meal only when adults. Among the latter, there are insects in the expression of autogeny.
that are obligatory blood feeders as adults, other insects that
are facultative blood feeders, and finally, those of which the
adult male is not hematophagous and only adult females MATERIAL AND METHODS
blood feed, such as mosquitoes.2
Mosquitoes of the family Culicidae are some of the most Mosquito strain. We serendipitously found autogenous
important arthropod vectors, transmitting a range of dis- egg production in a genetically diverse population of
eases to humans. Blood is the preferred source of nutrients Ae. aegypti that we collected from Kenya. This population
for mosquito females,6 but females can feed on plant nectar was created in the laboratory using samples of eggs col-
if far away from vertebrate hosts.7 This may also allow lected from villages around the districts of Kilifi and
22
populations to persist through times or places where blood Malindi, Kenya, in July 2010 (see Osei-Poku and others.
meals are not possible. In some mosquito species, females for detailed information on sampling site). There are two
are able to complete the first gonotrophic cycle without a main genetic forms of Ae. aegypti that are found in Africa
blood meal, a trait named autogeny, which can be particu- and across the rest of the tropics.
23 The coastal region of
larly important if hosts are scarce.2 Autogenous mosquitoes Kenya is the only area where these forms coexist. The
are able to store nutrients carried over from larval stages in population that we studied had clear white scaling on the
the fat body and use these in egg production.8 Most species first abdominal tergite, which suggests that they are the sub-
will still blood feed if a suitable warm-blooded host is avail- species Ae. aegypti aegypti. However, it should be cautioned
able, which can typically allow them to lay many more eggs that genetic studies have questioned whether this trait can dis-
23
with higher viability.9 tinguish the genetic forms.
The ability to lay eggs without a blood meal is the ances- In the laboratory, we separately reared eggs collected from
tral state for mosquitoes as other insect families related either the same oviposition traps or from a pool of ovipo-
to Culicidae are not blood feeders.10 Within the three sub- sition traps from the same area; only four egg collections
families that comprise the Culicidae, only the Culicinae and successfully survived until F2. We crossed females and males
Anophelinae feed on blood.2 Within these groups, autogeny from the four egg collections in every possible direction.
is common in mosquitoes of the genus Culex,11–13 but is rarer Equal numbers of the progeny of each cross were then com-
in Anopheles14 and Aedes mosquitoes.15–17 bined to create three cages of an outcrossed population, each
Very little is known about autogeny in Aedes aegypti, the with at least 300 mosquitoes. These were maintained for
primary vector of dengue and yellow fever. Autogeny has 11 generations.
Rearing conditions. We reared mosquitoes in a controlled
temperature room at 28°C (±1.5°C), 75% (±5%) relative
* humidity and a photoperiod of 12:12 (light: dark) hours. EggsAddress correspondence to Cristina V. Ariani, Department of
Genetics, University of Cambridge, Downing Street, CB2 3EH, used in each experiment were never more than 10 days old.
Cambridge, United Kingdom. E-mail: cristina.ariani@gmail.com The conditions in which we reared larvae varied slightly in
715
716 ARIANI AND OTHERS
each experiment (and are detailed in the following sections), were allowed to lay eggs autogenously but were subse-
but the standard procedures were as follows. To hatch eggs, quently given a blood meal as well. We had three replicate
we submerged filter papers containing eggs in deoxygenated cages for each treatment. We used ~1,300 eggs that were
water and then we density controlled first instar larvae to laid either autogenously or anautogenously by females from
8 larvae/100 mL of water and fed with desiccated liver the outcrossed population to establish the selected and the
powder (Oxoio). We either used 600 mL plastic containers unselected treatment, respectively. Seventy-three percent of
with 48 larvae, or 1,500 mL with 120 larvae. We added the autogenous eggs hatched, indicating that autogenous
350 mg of liver powder to the smaller containers and 750 mg eggs are viable. We reared larvae using 1,500 mL rearing
to the larger containers. Food was given every other day containers. Once females emerged, they were counted and
until pupation and water was changed whenever needed. the same number of individuals was kept in all cages. Usu-
We maintained a constant replicate number of 70 for the ally the number of anautogenous mosquitoes was greater
smaller containers, but the number of replicates of the larger than the autogenous; the surplus of the first was discarded
containers varied according to each experiment. When adults to ensure the density of individuals in all cages was identi-
emerged the standard procedure was to place 20 females and cal. We blood fed females from the control cages 8 days
20 males from each of the 600 mL containers into a small post adult emergence to allow autogenous egg laying before
cage (17.5 cm + 17.5 cm + 17.5 cm, BugDorm, Taichung, the blood meal.
Taiwan). See each experiment description for the procedure The effect of temperature. To test if temperature affects
used with adults from the 1500 mL containers. We placed a the autogeny trait we had two treatments, low temperature
50 mL plastic cup containing hay infusion and a strip of (22°C) and standard temperature (28°C). All rearing condi-
unbleached coffee filter paper in each cage to be used by tions, from hatching to adult emergence, followed the stan-
females as an oviposition site. We did some preliminary tests dard procedures, with 35 replicates at 22°C and 35 replicates
and mosquitoes showed a high preference for oviposition at 28°C. We ran both treatments at the same time but in
sites containing water that was infused with hay for a day two different controlled temperature rooms. We checked
instead of tap water. We placed cotton wool pads soaked in the oviposition sites daily and recorded the number of eggs
10% w/v fructose solution (Sigma-Aldrich, St. Louis, MO) on laid. We also measured wing size of females of both treat-
top of each cage, for adult mosquitoes to feed ad libitum. ments to test if a longer developmental time would result in
Frequency of autogeny in the outcrossed population and larger females.
body size. To estimate the frequency of autogeny in the out- Larval nutrition and competition. To investigate if larval
crossed population from Kenya, we reared larvae in 13 large nutrition affected the autogeny trait, we reared larvae from
(1,500 mL) containers, following the standard rearing proce- the outcrossed population (from eggs laid anautogenously)
dures previously described. Once emerged, 468 single pairings at low and high nutritional conditions. We provided the
of male and female were placed into 300 mL-paper cups. We same amount of food (liver powder) to larvae of both treat-
checked if eggs were laid in each cup until 10 days after adult ments but changed the density of larvae in each condition.
emergence (2 days after the last egg batch was seen). We For the low nutrition treatment, we had 48 larvae per
counted the number of eggs laid in each cup and collected 100 mL of water and for the high nutrition we used a
the adult females. density of 8 larvae per 100 mL of water. The former treat-
To test if body size correlated with the autogeny trait in ment generated a larval competition environment, where
Ae. aegypti, we measured the wing size (a proxy for body larvae had lower amounts of food available per individual.
size) of each autogenous female and twice as many anautoge- We used 600 mL plastic pots as rearing containers and the
nous females from the previous experiment. We carefully standard adult rearing procedures with 70 cages—35 cages
removed the right wing of each individual using dissection per treatment (20 adult females and 20 adult males in
tweezers and placed them on a microscope slide with a each cage). We checked daily and collected eggs until 10 days
cover slip. A photograph of each wing was taken. We mea- after emergence.
sured each wing from the apical notch to the tip, without Adult nutrition. To assess if adult nutrition would have
the fringe scales,24 using the program ImageJ.25 an effect on the ability of females to lay eggs autogenously,
Genetic variation in autogeny. To examine whether there we varied the fructose concentration given to adults, but
was genetic variation affecting autogenous egg laying, we larvae received the same amount of food. We reared larvae
tested if females reared from autogenous eggs were more from the outcrossed population stock using eggs that were
likely to lay eggs without a blood meal than control females laid after a blood meal. Adult rearing followed the standard
from a laboratory stock. We used eggs that were autogenously procedures as described previously, with 70 of the 600 mL
laid by females from the outcrossed population and eggs plastic containers. After adult emergence, each cage was
from Liverpool (LVP), a laboratory strain obtained from the assigned a specific concentration of fructose solution. Cotton
Malaria Research and Reference Reagent Resource Center wool pads soaked in the corresponding solution were placed
(MR4, ATCC, Manassas, VA). We reared larvae from each on top of each cage. We used 43 different concentrations of
strain in six 1,500 mL containers, which were placed in fructose solution (28 concentrations with two replicates and
three cages following the standard procedures until adult 15 concentrations with one replicate), ranging from 0% to
emergence. We recorded the number of eggs laid autoge- 17.5%. From 0% up to 7%, concentrations increased approxi-
nously in each cage. mately every 0.3% (i.e. 0%, 0.3%, 0.6%, 1%, etc.) with two
We also checked whether the autogeny trait would respond replicates (two cages per concentration). From 7.5% to 10%,
to short-term selection. We maintained a selected treatment concentrations raised every 0.5% also with two replicates.
where females were never blood fed (eggs were always laid From 10.5% to 17.5%, concentrations also raised every 0.5%
autogenously) and an unselected treatment, where females but with no replicates. This design was to ensure we would
FACTORS DETERMINING AUTOGENY IN THE MOSQUITO AE. AEGYPTI 717
be able to detect any fine differences in the autogeny trait We next examined whether the variation in autogeny
at low concentrations of fructose. Every day we checked if expression that we see within our Kenyan population is
eggs were laid and counted mosquito mortality. Cotton wool genetically determined. To do this, we tested whether the
pads were re-soaked in the respective fructose solution daily. progeny of autogenous mosquitoes were more likely to repro-
The experiment was stopped when no eggs were laid for duce autogenously than the rest of the population. We com-
2 consecutive days. pared the number of autogenous eggs laid in a selected
Statistical analysis. We used R version 2.15.1 (R Founda- treatment, which laid eggs autogenously and was never fed
tion for Statistical Computing, Vienna, Austria) to perform on blood, to controls that were fed on blood. The latter was
all tests and the package ggplot226 to plot most graphs. There allowed to lay eggs autogenously before receiving a blood
were many zeros in our data set caused by lack of autoge- meal. Across two generations of selection there was a trend
nous egg laying in some cages. To account for that, we fitted for the selected population to produce more autogenous eggs,
a zero-inflated Poisson regression model using the package but this was not statistically significant (ANOVA, effect of
pscl.27 We tested if a zero-inflated Poisson was the best selection regimen: F(1–9) = 3.68, P = 0.087; Figure 1C). To
model by comparing it to a Poisson generalized linear model check if autogeny would increase in response to longer-term
(GLM) using a Vuong Statistic for non-nested models. In selection treatment, we maintained the cages for another three
all cases a zero-inflated Poisson was preferred. We fitted a generations. Only a small number of mosquitoes remained
zero-inflated Poisson model to test whether there was a main in a single selected and control cage by this stage, and the
effect of temperature, larval nutrition, fructose concentra- number of eggs laid autogenously was the same between
tion, and adult age on the number of eggs laid autogenously. treatments (13 and 14 eggs, respectively; Figure 1C). There-
fore, although there is likely genetic variation within this
RESULTS population, the autogeny trait does not rapidly change in
response to selection.
Aedes aegypti can lay eggs autogenously at a low fre- Females lay more eggs autogenously when kept at 28°C.
quency. In a genetically diverse population that originated Temperature had a strong effect on autogenous egg laying.
from Ae. aegypti from Kenya, we found that 3.2% (N = 468) Females reared at 28°C laid a mean of 10.4 eggs in each
of females were able to lay eggs autogenously. The mean cage, compared with 0.2 eggs at 22°C (zero-inflated Poisson
number of eggs laid by the autogenous females was 18.2 GLM: df = 4, P < 0.0001, Figure 2A). At lower tempera-
(SD 5.7; Figure 1A). In other species, the body size of ture, we found eggs in only one cage (N = 35), although
mosquito females has been previously correlated with the at higher temperature we encountered eggs in 16 cages
autogeny trait.15 Using wing size as a proxy for body size, (N = 35) (Fisher’s exact test, P < 0.001). This pattern cannot
we found a trend for autogenous females to be larger, how- be explained by changes in body size as the adults were
ever this was not statistically significant (analysis of variance larger at the lower temperature (ANOVA, F(1–153) = 119.3,
[ANOVA], F1, 44 = 2.27, P = 0.13; Figure 1B). R
2 = 0.43, P < 0.0001; Figure 2B). This increase in size may
Genetic variation in the expression of autogeny. To exam- result from a longer development time between hatching
ine whether the autogeny trait is genetically inherited, we and adult emergence, which took 13 days at 22°C—5 days
compared autogeny expression between our Kenyan popula- longer than at 28°C. Because of this extended developmen-
tion and a laboratory line that originated from West Africa. tal time at lower temperature, we maintained the cages for
We found that the genotypes differed in their abilities to 20 days after adult emergence to ensure that a delayed egg
reproduce autogenously, with the Kenyan mosquitoes laying laying was not affecting our results.
511 autogenous eggs and the laboratory stock producing no Well-nourished larvae laid more eggs autogenously. High
eggs (three cages of Kenyan mosquitoes produced 78, 249, larval nutrition increases the ability of females to lay eggs
and 184 eggs, and none of the three cages of the laboratory autogenously. We reared larvae in high and low den-
stock laid eggs). sities with the same amount of food, therefore the low
Figure 1. Frequency of autogeny, the effects of body size and short-term selection on the autogeny trait in an Aedes aegypti population from
Kenya. (A) Number of eggs laid autogenously by individual autogenous females. Females that did not lay autogenously are not shown. (B) Wing
size, as a proxy for body size, of autogenous and anautogenous females. (C) The number of autogenous eggs laid by mosquitoes selected for the
autogeny trait compared with an unselected control. The number of mosquitoes in each generation declined, explaining the overall decline in the
number of eggs laid.
718 ARIANI AND OTHERS
Figure 2. The effects of temperature, larval nutrition, and adult nutrition on the autogeny trait in an Aedes aegypti population from
Kenya. (A) Mosquitoes reared at 28 °C laid more autogenous eggs than at 22 °C. (B) Females’ body size, measured as wings length, was
larger when reared at 22 °C compared with 28 °C. (C) Females that were well nourished during the larval stage laid more autogenous
eggs than females that received a poor diet. (D) The number of eggs laid autogenously is greater when adult females are fed with higher
fructose concentrations.
density larvae received proportionally more food. Females GLM, main effect days post emergence: df = 6, P < 0.0001;
that were well nourished during larval stages laid more Figure 3B).
eggs (zero-inflated Poisson GLM: df = 4, P < 0.001,
Figure 2C) and more frequently—we found eggs in
27 cages (N = 35) of the high nutrition treatment and DISCUSSION
only eight in low nutrition cages (N = 35) (Fisher’s exact
test, P < 0.001). We found that autogenous egg production in Ae. aegypti
Sugar feeding greatly increases the number of eggs laid is highly dependent on environmental conditions. High tem-
autogenously. The number of eggs laid autogenously was con- peratures, good larval nutrition, and adult sugar feeding all
siderably greater when adult females fed on high fructose greatly increase the ability of females to lay eggs autogenously.
concentrations (zero-inflated Poisson GLM: df = 4, P = 0.0001,
Figure 2D). No eggs were laid in cages that were given < 1.6%
fructose, and the majority of cages with over 8% fructose had
eggs. Interestingly, among the cages where eggs were laid
there was no strong effect of fructose concentration, suggest-
ing that sugar feeding above a particular threshold (in this
case 1.6%) may primarily affect the probability of auto-
geny rather than number of eggs produced by the autoge-
nous females.
Age influences the ability to lay eggs autogenously. We
used the females from the adult nutrition experiment to
examine the effect of age on autogenous egg laying.
Females started laying eggs autogenously 3 days post-
emergence and stopped by the ninth day post-emergence Figure 3. Age affects the probability of Aedes aegypti females
from an outcrossed population from Kenya laying eggs autogenously.
(Figure 3A), with the peak of egg laying on Day 4 post-
The effect of mosquito age on the proportion of cages with autoge-
emergence. We found that younger females laid a greater nous eggs (out of 70 cages) (A) and the number of autogenous eggs
number of eggs than older females (zero-inflated Poisson in each cage (B).
FACTORS DETERMINING AUTOGENY IN THE MOSQUITO AE. AEGYPTI 719
Furthermore, the trait varies genetically and only certain geno- Temperature had a strong effect on the expression of
types of Ae. aegypti are able to reproduce autogenously. autogeny in Ae. aegypti, with 50 times more autogenous
The frequency of autogeny in an outcrossed population eggs laid at 28°C than 22°C. This is similar to Cx. salinarius,
of Ae. aegypti from Kenya was 3.2%. This suggests that which is obligatorily autogenous at warm temperatures, but
autogeny alone is unlikely to sustain Ae. aegypti populations facultatively autogenous at colder temperatures.12 In Culex
in Kenya. In Uganda, however, the trait was found in 34% tarsalis autogeny is suppressed below 21°C and reaches
of females.18 In Aedes albopictus and Culex annulirostris, maximum expression at 32°C.35 Lower temperatures resulted
the trait was detected in 5% to 8% of wild-caught indi- in a slower developmental time, which was also observed
viduals,28,29 whereas 27% of Culex salinarius, 87% of Culex in Cx. pipiens.36 We found that the females’ body size was
pipiens f. molestus, and 100% of Ochlerotatus atropalpus were larger when reared at 22°C, which suggests that the effect of
autogenous.12,30,31 Although it is clear that there are large temperature on autogenous egg laying is not purely caused
differences in the importance of autogeny across species, by it resulting in more poorly resourced mosquitoes.
these exact numbers must be treated with care. First, the Larval nutrition is another important factor affecting
comparison between studies is difficult as each study rear autogenous egg laying in Ae. aegypti. Females that were
mosquitoes under different conditions and it is also difficult well nourished during larval stages laid more eggs autoge-
to extrapolate these estimates to wild populations, where nously. The importance of larval nutrition in the expres-
natural environment is dramatically different to laboratory sion of autogeny has been reported in other mosquito
conditions. Furthermore, our population has been reared in species.19,31,37 Following blood feeding, amino acid titers
the laboratory for 11 generations; therefore, it is possible increase in the hemolymph triggering a cascade of metabolic
that selection in the laboratory may have altered the rate of events that culminates with eggs production.38 It is likely that
autogeny relative to wild Kenyan populations. In addition, autogenous individuals are able to mobilize enough amino
some females may not have laid eggs autogenously simply acids stored in the fat body during larval stages to trigger
because they did not mate or lacked the correct cues to vitellogenesis.39 The mechanism that facilitates this event is
oviposit in our rearing cups. still unknown.
The frequency of autogeny in a population is likely to be Because larval nutrition largely affects body size and is
associated with host availability, with the frequency increas- one of the main factors influencing the autogeny trait,
ing if hosts are scarce.2 We created the outcrossed popula- larger females might be expected to be the most likely
tion in our laboratory with eggs collected in peri-domestic to reproduce autogenously, as is the case for species like
areas of Kenya. Even though humans are present around the Aedes bahamensis and Oc. atropalpus.15,19 However, this is
collection sites and it is unlikely that other vertebrates are not always the case; there was no correlation between body
not available, it is possible that autogeny is used as a repro- size and autogeny in a selected strain of Ae. albopictus from
ductive strategy by mosquito females from these areas. More- Japan.16 Mosquitoes’ body size also correlates with protein
over, the precise frequency of autogeny may have changed as content, which is generally carried over from larval stages.24
a result of inadvertent selection in the laboratory. In Ae. aegypti, there was a trend in our data suggesting that
Autogeny in Ae. aegypti has a genetic basis. We com- larger females lay more autogenous eggs but this was not
pared a laboratory stock and an outcrossed population from statistically significant. There are two possible explanations
Kenya. Only the latter laid eggs autogenously, suggesting for our results: it may be that our sample size was small and
that even if the environmental conditions are favorable, it impaired the detection of the correlation between body
autogeny only occurs in certain genotypes. We also tested size and autogeny expression, or in Ae. aegypti nutrition
if there was heritable variation in autogeny expression in may have a role in autogeny that is independent of body
our Kenyan population. Selection on the trait did generate size. Further studies with larger sample sizes are necessary
an increase in the number of autogenous eggs, although this to clearly explain this.
did not reach statistical significance. When we maintained Adult nutrition also affected the autogenous egg laying—
the cages for a further three generations we saw a decline females that were offered a higher fructose concentration
in the number of eggs laid autogenously, indicating that laid more eggs. There was a threshold fructose concentration
the trait does not rapidly respond to selection. Furthermore, below which females did not lay eggs autogenously. Aedes
the number of eggs laid per female is much lower when bahamensis and Cx. tarsalis only laid eggs autogenously if
laid autogenously,32,33 which may explain the decline in the females had access to sugar.15,21 Caloric intake also deter-
number of females across generations. Perhaps the autogeny mined if Ae. albopictus would lay eggs autogenously but
trait is an adaptation to allow populations to persist in times it did not affect the number of eggs laid.40 The concentra-
when hosts are temporarily unavailable, but it is not suffi- tion of sugar in adult females is responsible for either
cient to continue the population across multiple genera- stimulating or preventing follicular resorption, a strategy
tions without blood feeding. The genetic basis of autogeny used by mosquitoes to reallocate nutrients from reproduc-
in Ae. aegypti is not known. In Ae. albopictus, the trait is tion to other physiological activities when the availability
dominant and multigenic, with quantitative trait loci affect- of carbohydrates is low.41,42 Thus, fecundity is greater when
ing autogeny overlapping with loci affecting follicle size females feed on higher sugar concentrations.41 The peak of
(the proxy for autogeny) and body size.16 In Oc. atropalpus, egg laying was at Day 4 post adult emergence. Aedes aegypti
autogeny appears to have a simple genetic basis and is normally lay eggs about 4 days after having a blood meal,
affected by a single dominant autosomal locus, with modifiers when egg maturation is complete. This suggests that in
affecting the level of fecundity.34 To our knowledge, it is autogenous mosquitoes vitellogenesis may somehow be
unknown which genes are responsible for autogeny in any triggered upon emergence as long as adult females have
mosquito species. access to sugar.13
720 ARIANI AND OTHERS
There are other factors affecting autogeny in other mos- 14. Sweeney A, Russell R, 1973. Autogeny in Anopheles amictus
quito species that have not been addressed in this study hilli. Mosq News 33: 467–468.
43,44 15. O’Meara GF, Larson VL, Mook DH, 1993. Blood feeding andand should be investigated, such as photoperiodicity, the
autogeny in the peridomestic mosquito Aedes bahamensis
effect of mating and the consequent transference of the (Diptera: Culicidae). J Med Entomol 30: 378–383.
substance of the male accessory gland to females.40,45 16. Mori A, Romero-Severson J, Black WC, Severson DW, 2008.
We provided data for the understanding of the occurrence Quantitative trait loci determining autogeny and body size
of the rare autogeny trait in a highly urban mosquito. We in the Asian tiger mosquito (Aedes albopictus). Heredity 101:
75–82.
conclude that environmental factors, such as temperature and 17. Thomas V, Leng YP, 1972. The inheritance of autogeny in Aedes
nutrient availability to both larvae and adults play a major role (Finlaya) togoi (Theobald) from Malaysia and some aspects
at the expression of autogeny, but this is not sufficient for of its biology. Southeast Asian J Trop Med Public Health 3:
autogenous egg production if females lack a genetic predispo- 163–174.
sition for the trait. The ideal conditions for autogeny expres- 18. Trpis M, 1977. Autogeny in diverse populations of Aedes aegypti
from East Africa. Tropenmed Parasitol 28: 77–82.
sion are very specific, therefore it is unclear how frequently 19. Telang A, Li Y, Noriega FG, Brown MR, 2006. Effects of larval
environmental conditions in the wild will allow autogeny. nutrition on the endocrinology of mosquito egg development.
J Exp Biol 209: 645–655.
Received July 28, 2014. Accepted for publication November 20, 2014. 20. Corbet P, 1967. Facultative autogeny in arctic mosquitoes. Nature
215: 662–663.
Published online February 2, 2015. 21. Su T, Mulla MS, 1997. Physiological aspects of autogeny in
Financial support: CVA is supported by a Cambridge Overseas Trust Culex tarsalis (Diptera: Culicidae): influences of sugar-feeding,
Studentship. FMJ is supported by a Royal Society Research Fellow- mating, body weight, and wing length. J Vector Ecol J Soc
ship and ERC grant Drosophila Infection. PJ is supported by ERC Vector Ecol 22: 115–121.
grant 281668 Drosophila Infection. 22. Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM, 2012. Deep
sequencing reveals extensive variation in the gut microbiota
Authors’ addresses: Cristina V. Ariani, Sophia C. L. Smith, Katherine of wild mosquitoes from Kenya. Mol Ecol 21: 5138–5150.
Short, Punita Juneja, and Francis M. Jiggins, Department of Genetics, 23. Brown JE, McBride CS, Johnson P, Ritchie S, Paupy C, Bossin
University of Cambridge, Cambridge, UK, E-mails: c.ariani@gen.cam H, Lutomiah J, Fernandez-Salas I, Ponlawat A, Cornel AJ,
.ac.uk, ss2192@cam.ac.uk, kas214@hotmail.co.uk, p.juneja@gen.cam Black WC, Gorrochotegui-Escalante N, Urdaneta-Marquez
.ac.uk, and f.jiggins@gen.cam.ac.uk. Jewelna Osei-Poku, Department L, Sylla M, Slotman M, Murray KO, Walker C, Powell JR,
of Parasitology, Noguchi Memorial Institute for Medical Research, 2011. Worldwide patterns of genetic differentiation imply
Accra, Ghana, E-mail: j.osei-poku@hotmail.co.uk. multiple “domestications” of Aedes aegypti, a major vector
of human diseases. Proc Biol Sci 278: 2446–2454.
24. Van Handel E, Day JF, 1989. Correlation between wing length
REFERENCES and protein content of mosquitoes. J Am Mosq Control Assoc
5: 180–182.
1. Adams TS, 1999. Hematophagy and hormone release. Ann 25. Schneider CA, Rasband WS, Eliceiri KW, 2012. NIH Image to
Entomol Soc Am 92: 1–13. ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.
2. Lehane MJ, 2005. The Biology of Blood-Sucking Insects. 26. Wickham H, 2009. ggplot2: Elegant Graphics for Data Analysis.
Cambridge: Cambridge University Press. New York: Springer.
3. Garrett-Jones C, 1951. The Congo Floor Maggot, Auchmeromyia 27. Zeileis A, Kleiber C, Jackman S, 2008. Regression models for
luteola (F.), in a laboratory culture. Bull Entomol Res 41: count data in R. J Stat Softw 27: 1–21.
679–708. 28. Chambers GM, Klowden MJ, 1994. Nutritional reserves of
4. Leak SGA, 1999. Tsetse biology and Ecology: Their Role in the autogenous and anautogenous selected strains of Aedes
Epidemiology andControl ofTrypanosomosis.Wallingford:CABI. albopictus (Diptera: Culicidae). J Med Entomol 31: 554–560.
5. Zeledón R, Rabinovich JE, 1981. Chagas’ disease: an ecological 29. Kay BH, Edman JD, Mottram P, 1986. Autogeny in Culex
appraisal with special emphasis on its insect vectors. Annu Rev annulirostris from Australia. J AmMosq Control Assoc 2: 11–13.
Entomol 26: 101–133. 30. Vinogradova EB, Karpova SG, 2006. Cultivation of the mosquito
6. Briegel H, 2003. Physiological bases of mosquito ecology. J Vector Culex pipiens pipiens f. molestus (Diptera, Culicidae) without
Ecol 28: 1–11. blood feeding. Parazitologiia 40: 306–311.
7. Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark 31. Telang A, Wells MA, 2004. The effect of larval and adult
GG, Strickman D, Kittayapong P, Edman JD, 2000. Longitu- nutrition on successful autogenous egg production by a mos-
dinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand quito. J Insect Physiol 50: 677–685.
and Puerto Rico: blood feeding frequency. J Med Entomol 32. O’Meara GF, Evans DG, 1973. Blood-feeding requirements of
37: 89–101. the mosquito: geographical variation in Aedes taeniorhynchus.
8. Clements AN, 1992. The Biology of Mosquitoes: Development, Science 180: 1291–1293.
Nutrition, and Reproduction. London: Chapman & Hall. 33. O’Meara GF, Edman JD, 1975. Autogenous egg production
9. Junkum A, Choochote W, Jitpakdi A, Leemingsawat S, in the salt-marsh mosquito, Aedes taeniorhynchus. Biol Bull
Komalamisra N, Jariyapan N, Boonyatakorn C, 2003. Com- 149: 384–396.
parative studies on the biology and filarial susceptibility of 34. O’Meara G, Craig G Jr, 1969. Monofactorial inheritance of
selected blood-feeding and autogenous Aedes togoi sub-colonies. autogeny in Aedes atropalpus. Mosq News 29: 14–22.
Mem Inst Oswaldo Cruz 98: 481–485. 35. Brust RA, 1991. Environmental regulation of autogeny in Culex
10. Pawlowski J, Szadziewski R, Kmieciak D, Fahrni J, Bittar G, tarsalis (Diptera: Culicidae) from Manitoba, Canada. J Med
1996. Phylogeny of the infraorder Culicomorpha (Diptera: Entomol 28: 847–853.
Nematocera) based on 28S RNA gene sequences. Syst Entomol 36. Strickman D, Fonseca DM, 2012. Autogeny in Culex pipiens
21: 167–178. complex mosquitoes from the San Francisco Bay Area. Am J
11. Spielman A, 1957. The inheritance of autogeny in the Culex Trop Med Hyg 87: 719–726.
pipiens complex of mosquitoes. Am J Hyg 65: 404–425. 37. Reisen W, Milby M, Bock M, 1984. The effects of immature
12. Tveten MS, Meola RW, 1988. Autogeny in Culex salinarius from stress on selected events in the life history of Culex tarsalis.
Texas, Florida and New Jersey. J Am Mosq Control Assoc Mosq News 44: 385–395.
4: 436–441. 38. Hansen IA, Attardo GM, Park J-H, Peng Q, Raikhel AS,
13. Provost-Javier KN, Chen S, Rasgon JL, 2010. Vitellogenin gene 2004. Target of rapamycin-mediated amino acid signaling
expression in autogenous Culex tarsalis. Insect Mol Biol 19: in mosquito anautogeny. Proc Natl Acad Sci USA 101:
423–429. 10626–10631.
FACTORS DETERMINING AUTOGENY IN THE MOSQUITO AE. AEGYPTI 721
39. Attardo GM, Hansen IA, Raikhel AS, 2005. Nutritional regulation 43. Sota T, Mogi M, 1994. Seasonal life-cycle and autogeny in
of vitellogenesis in mosquitoes: implications for anautogeny. the mosquito Aedes togoi in northern Kyushu, Japan, with
Insect Biochem Mol Biol 35: 661–675. experimental analysis of the effects of temperature, photope-
40. Chambers GM, Klowden MJ, 1996. Distention and sugar feeding riod and food on life-history traits. Res Popul Ecol (Kyoto)
induce autogenous egg development by the Asian tiger mos- 36: 105–114.
quito (Diptera:Culicidae). J Med Entomol 33: 372–378. 44. Sota T, Mogi M, 1995. Geographic variation in the expression of
41. Clifton ME, Noriega FG, 2011. Nutrient limitation results in juve- autogeny in Aedes togoi (Diptera: Culicidae) under different
nile hormone-mediated resorption of previtellogenic ovarian temperature and photoperiod conditions. J Med Entomol 32:
follicles in mosquitoes. J Insect Physiol 57: 1274–1281. 181–189.
42. Clifton ME, Noriega FG, 2012. The fate of follicles after a blood 45. O’Meara GF, Evans DC, 1977. Autogeny in saltmarsh mos-
meal is dependent on previtellogenic nutrition and juvenile quitoes induced by a substance from the male accessory gland.
hormone in Aedes aegypti. J Insect Physiol 58: 1007–1019. Nature 267: 342–344.
View publication stats