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348 Journal of Vector Ecology December2011
Narrow-sense heritability of body size and its response to
different developmental temperatures in Culex quinquefasciatus (Say
1923)
Filiz Gunay, Bulent Alten, and Ergi D. Ozsoy
Hacettepe University, Science Faculty, Department of Biology,
Evolutionary and Ecological Genetics Laboratory (EEGL), 06800
Beytepe, Ankara, Turkey, [email protected]
Received 6 May 2011; Accepted 26 July 2011
ABSTRACT: Body size is an important trait involved in overall
fitness through its effects on mating success, fecundity, resource
acquisition and mortality, and desiccation resistance. In this
study, we raised inbred Culex quinquefasciatus mosquito cohorts at
different developmental temperatures of 20, 23, and 27 C. As an
indicator of the amount of genetic variation in body size, we
estimated the narrow-sense heritability of body sizes defined as
wing aspect ratios. Our results show that narrow-sense heritability
of the body size increased as the developmental temperature
increased. We also detected the presence of strong
genotype-by-environment (G x E) interaction from low
cross-environmental correlations. The body size of each temperature
regime followed the general rule that higher temperatures produce
smaller individuals. We suggest that the increase in genetic
variation with increasing temperature might be due to an unleashing
of the cryptic genetic variation of the putative genes affecting
body size. We conclude that this increase in genetic variation
tracking the environmental (developmental temperature) change could
have considerable implications for the distribution and range
expansion of Cx. quinquefasciatus, especially in warmer
environments. Journal of Vector Ecology 36 (2): 348-354. 2011.
Keyword Index: Culex quinquefasciatus, body size, narrow-sense
heritability, genotype-by-environment interaction.
INTRODUCTION
Members of the Culex (Culex) pipiens L. complex are among the
best-studied mosquitoes because of their worldwide distribution,
close association with humans, and importance as nuisances or
vectors of pathogens of human and animal diseases. There are
extensive behavioral, physiological, and morphological variations
and intricate interfertility among local populations of the forms
in this complex. Culex quinquefasciatus Say, a vector of avian
malaria (Goff and van Riper III 1980), West Nile virus (Reisen et
al. 2004), bancroftian filariasis, Chikungunya, and St. Louis
encephalitis (Marquardt et al. 2005), is widely distributed in the
tropical and subtropical areas of the world. It occurs in all
climatic zones, ranging from forest to semi-desert.
Variation in growth rates in insects may often be adaptive
(Arendt 1997). Body size varies continuously because of the effects
of natural selection on the size-dependency of resource acquisition
and mortality rates (Chown and Gaston 2010). In addition,
temperature is a critical factor for insects, directly affecting
lifespan, mortality, and development rates, which can govern
phenotypic alterations including changes in morphology (Sibly and
Atkinson 1994, Debat et al. 2003, Maharaj 2003).
The fecundities of different species show very different types
of dependence on environmental variables. Small individuals may
survive and reproduce better when food is limited because they need
less food to sustain themselves (Dingle 1992, Blanckenhorn et al.
1994). On the other hand, larger individuals may survive better
when there is no food at all, e.g., during hibernation if body size
is correlated with
nutrient reserves (Ohgushi 1996). As a generally accepted
guideline, increased temperature results in higher growth rates,
shorter development times, and smaller adult size in insects and
other ectotherms (Sibly and Atkinson 1994). The direct effect of
temperature on metabolic rates sets limits for growth rates and,
since size is typically less flexible, for development times (Nylin
and Gotthard 1998). Reaction norm is an important and highly
operative concept about the change of genotypic expression through
different environments (Schlichting and Pigliucci 1998). It also
defines a panel of environmental expression profiles that can be
used to assess genotype-by-environment (G x E) interaction (Mackay
and Anholt 2007).
Narrow-sense heritability (h2) is a useful and measurable
concept to assess the amount of genetic contribution to phenotypic
variation in a trait that is influenced by many genes with additive
effects (Falconer and Mackay 1996, Lynch and Walsh 1998). It also
provides an idea of the capacity to respond to selection when the
environment changes. When the amount of genetic variation that is
expressed as narrow-sense heritability is relatively low, it is
assumed that considerable selection operates on the trait in
question (Falconer and Mackay 1996, Lynch and Walsh 1998).
In this study we present our estimations of narrow-sense
heritability (h2) of body sizes that were determined as wing aspect
ratios in mosquitoes raised at different developmental temperatures
and, as the heritabilities were obtained in particular
environments, we show them in the perspective of a reaction norm
with a focus on the degree of G x E. We also determine the degree
of G x E quantitatively from the magnitude of the
cross-environmental correlations
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Vol.36,no.2 Journal of Vector Ecology 349
obtained for the different developmental temperatures in our
experiments.
MATERIALS AND METHODS
Maintenance of laboratory coloniesThe S. Lab colony used in this
study was previously
reared in France (ISEM), which originated from California in the
1980s. Egg rafts from the colony were transferred to the Ecological
Research Laboratory of Hacettepe University (ESRL) in Ankara,
Turkey, in 2005. The rearing and feeding of adults and larvae
followed the methods of Kasap and Kasap (1983) with a temperature
271 C, 605 RH%, and 14:10 h (L:D) photoperiod. Individuals used in
the experiments were obtained from the same generation (F30).
Maintenance of cohorts in the climate chambers The colonization
history and techniques to maintain
them are as described in Gunay et al. (2010). Individuals were
all obtained from the same generation (F30). Three replicates of
750 1st instar larvae were transferred into standard polyethylene
27x16x17 cm cups containing 1 liter of distilled water on the
subsequent day of their oviparity. The cups were placed in five
climate chambers programmed at five different temperatures (15, 20,
23, 27, and 30 C) and exposed to a 14:10 (L:D) photoperiod with a
constant relative humidity of 60%. Based on their developmental
stage, the larvae were fed each day with 0.01-0.1 g sinking
Tetramin fish food. Pupal development was checked daily and the
pupae were counted. After pupation, 100 female and 100 male adults
were selected when both sexes were emerging evenly, and then placed
in 20x20x20 cm cloth cages to reproduce in each chamber, with
plastic cups containing distilled water provided as oviposition
sites for each replicate at each temperature. Females were fed with
fresh chicken blood every four days for 2 h. Experiments for this
study lasted for three generations, (F0, F1, and F2), thus we
generated as many fourth generation (F3) adults as possible using
the same standard rearing method. All F3 pupae were separated into
glass vials before eclosion. From the virgin adults obtained, the
following procedure was monitored.
Maintenance of F3 cohorts in climate chambers One virgin male
and five virgin females were
transferred to 7x7 cm polyethylene cups with distilled water at
the bottom for oviposition and were placed into the rearing
chambers. In order to minimize their stress, females were
artificially fed with fresh chicken blood using the glass apparatus
from Kasap et al. (2003), during their optimum time preferences
from midnight to 02:00 every day until at least one of them
produced fertilized eggs. Despite all our efforts due to the
decrease in the survival rates through generations (Gunay et al.
2010), we did not succeed in producing enough replicates from the
extreme temperatures of 15 and 30 C. We recovered 15 replicates for
20, 23, and 27 C; 15 virgin males were mated with virgin females
and the offspring of just one female were
used for wing aspect ratio estimations.
Body size: wing measurementsAs an indicator of body size, wing
aspect ratios
(WAR) were estimated. The left wings of F3 males (fathers, 4th
generation) and F4 males (sons, 5
th generation) were mounted on slides in Entellane and
photographed. Length of the left wing was measured as the distance
from the basal of the alula to the apical of the third radius vein
(R3), which is shown as a line from 4th to 11th landmarks in Figure
1. In addition, centroid sizes were estimated using 20 landmarks
out of those 22 suggested by Aytekin et al. (2009) (Figure 1). The
wing aspect ratio was defined as the ratio of the squared wing
length to the wing centroid size. Centroid size was preferred to
wing area in these estimations to minimize the measurement error
(Debat et al. 2003). Only the wing of the males were used in our
estimations, as the environmental variance is known to be reduced
20% in males compared to that of females (Reeve and Robertson
1954). The heritability design rested on the male measurements as
below. Mean body sizes and coefficients of variation (CV) of
fathers and sons developed at respective temperatures were
estimated. Coefficient of variation were compared using F ratio
statistics, CV2X/CV
2Y, for NX-1 and NY-1 (N: sample size)
degrees-of-freedom, in which X and Y were the coefficients of
two samples (of the fathers and sons developed at different
temperature regimes in our case) (Lewontin 1966).
Narrow-sense heritability (h2) and the reaction normNarrow-sense
heritability was estimated for three
temperature regimes (i.e., 20, 23, and 27 C) with the
offspring-on-parent regression method (Falconer and Mackay 1996).
Fifteen single male-female matings were realized for each
temperature regime. Among the fourth generation offspring, one
adult male per each mating was picked up randomly. Thus, fifteen
sons per mating were obtained. Their wing components were measured
as defined above and regressed on their fathers. The simple
regression equation is Y (sons) = ab + X (fathers), and the
regression coefficient (b) can be related to narrow-sense
heritability (h2) as b = h2/2, hence h2 = 2b (Falconer and Mackay
1996). Reaction norms for narrow-sense heritability (h2) were
obtained by plotting the respective values of the heritabilities
against the different temperature regimes at which cohorts
developed.
RESULTS
The sample means and their standard errors, and the coefficient
of variations (CV) for wing aspect ratios of the fathers and sons
are shown in Table 1. Body size values as measured by wing aspect
ratios followed the general rule that the lower the temperature,
the greater the size, both in fathers and the sons (Table 1). As
for the correlation coefficients (CV), it is evident that the body
sizes did not vary much with varying developmental temperatures. We
also tested, for both fathers and sons, if there were significant
differences in the variability (i.e., CV) of body
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350 Journal of Vector Ecology December2011
Figure 1. Location of the 20 landmarks on the wing of male Cx.
quinquefasciatus.
Figure 2. The reaction norms of narrow-sense heritability (h2)
and coefficient of variation (CV) of fathers and their sons across
different developmental temperatures.
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Vol.36,no.2 Journal of Vector Ecology 351
sizes between pairs of temperature regimes. It seems there is no
significant difference between any pair of father or son
comparisons, or between father-son comparisons at their
developmental temperatures (F ratio values in Table 1, as
CV2X/CV
2Y). Total phenotypic variability levels thus seem
to be very similar across the developmental temperature gradient
of our study. However, the most remarkable result for our study
context is that heritability shows a distinct pattern of increasing
temperature effect. Table 2 shows the offspring- (sons) on-parent
(fathers) regression coefficients (b) for body sizes (wing aspect
ratios, WAR) and the values of narrow-sense heritabilities (h2)
estimated from them. The range of the h2 values lies between 0.152
(20 C) and 0.582 (27 C). The highest value of h2 obtained, i.e.,
that of 27 C developmental temperature which is almost four times
more than that of 20 C, clearly points to a higher temperature -
higher heritability effect (Table 2; h2). Figure 2 shows the
reaction norms for h2 and CVs of fathers and sons across all
developmental temperatures. Figure 2 indicates that although the
total (i.e., genetic and environmental components combined)
phenotypic variation expressed as coefficient of variation shows
little change across the
temperatures, the increase of the heritability with increasing
temperatures is prominent. Because we have used an inbred strain,
genotype-by-environment interaction (G x E) might be revealed from
the pattern of the reaction norm in the heritability, taking our
strain as genotype (i.e., regarding it an individual sample of the
whole genome of the Cx. quinqefasciatus), we performed
cross-environment correlation analyses between the phenotypic
expressions (i.e., WAR) of body size of the sons raised at
different temperatures for the heritability analyses. The idea was
that if there were G x E correlations between environmental pairs
(i.e., correlations using the WAR values of individuals raised at
different temperatures), they would be less than unity (Mackay and
Anholt 2007). Table 2 also shows the results of these Pearson
product moment correlation estimations (Sokal and Rohlf 1995) under
the Correlation. All correlation coefficients (r) are less than
one, and hence a strong indication of a G x E. While two
correlations with 23 C sons give negative values (r: -0.185 and
-0.265, for 20-23 C and 23-27 C, respectively), only the
correlation between 20 C and 27 C was positive (Table 2).
DISCUSSION
Body size is one of the most important features of organisms,
affecting key fitness traits such as mating success and fecundity
(Reeve et al. 2000), and determines the size dependency of resource
acquisition and mortality rates on which natural selection can act
(Chown and Gaston 2010). Many ecological factors shape body size in
insects, growth temperature being one of the most effective through
its effects on the length of aquatic life span, mortality, and
developmental rates, which are in turn determinative of overall
fitness (Sibly and Atkinson 1994, Debat et al. 2003, Maharaj 2003).
In this context, genetic variation and its expression underlining
body size should be directly related to the response and evolution
of the organism in general.
In this study, we raised a highly inbred strain of Cx.
Table 1. Wing aspect ratio means (FWAR: Fathers wing aspect
ratio, SWAR :Sons wing aspect ratio) and their standard errors, and
coefficient of variations as percentages of (CV) fathers and their
sons at the respective developmental temperatures. Variability
differences as CV test values obtained from F ratio tests are also
shown for both fathers and sons, and for father-son pairs (ns: not
significant, P>0.05).
Mean SE CV Fathers Sons CVfathers2/CVsons2
FWAR20C 2.261 0.042 7.263
SWAR20C 2.215 0.035 6.241CV202/CV232:
1.366 nsCV202/CV232:
0.345 ns 20 C: 1.354 ns
FWAR23C 2.220 0.035 6.214
SWAR23C 2.062 0.056 10.619CV202/CV272:
1.248 nsCV202/CV272:
0.592 ns 23 C: 0.342 ns
FWAR27C 1.998 0.033 6.502
SWAR27C 2.035 0.042 8.114CV232/CV272:
0.913 nsCV232/CV272:
1.713 ns 27 C: 0.642 ns
Table 2. Estimations of narrow-sense heritability (h2). b:
regression coefficient between fathers and sons, genotype
environment interaction as Correlation (r): cross-environmental
correlations between sons of different temperatures; subscripts for
r-values signify respective temperatures (WAR: Wing Aspect Ratio).
ns: not significant, P>0.05.
b h2 Correlation (r)
20 C WAR 0.076 0.152 r20-23: -0.185 ns
23 C WAR 0.210 0.420 r20-27: 0.005ns
27 C WAR 0.291 0.582 r23-27: -0.265ns
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352 Journal of Vector Ecology December2011
quinquefasciatus at different developmental temperatures and
estimated body size and its narrow-sense heritability (h2) for each
temperature. Body sizes were expressed as the male wing aspect
ratios, a very useful index for predicting body size as a function
of wing length and an associated geometrical area parameter, the
centroid size. Narrow-sense heritabilities were estimated using the
offspring-on parent regression method, which is one of the most
widespread of the classical heritability measurements
available.
Overall, our results point to some remarkable aspects. First, as
shown in Table 1, mean body size as measured by wing aspect ratios
conform to the general observation (i.e., Bergmanns rule) that when
temperature is increased, body size is decreased accordingly. This
is true for the fathers across the entire temperature range with
the sons less so, with the lowest temperature (20 C) mediating the
lowest size and the remaining temperatures (23 C and 27 C) not in
decreasing size order. This may be due to the introduction of some
experimental variance. Clearly these sons would have shown the same
temperature response if that part of the experiment was repeated,
as the difference in size between 23 C and 27 C sons is small
compared to the difference between the sizes at 23 C (or 27 C) for
sons and the size of the sons of the lowest temperature (20 C).
Phenotypic variation as expressed by coefficients of variation (CV)
is considerably lower across the developmental temperatures in our
study. Although the inclusion of more thermal regimes may change
the range of the lower CV values, we think that the overall picture
would have been mostly the same as we included three developmental
temperatures in increasing order in the current study. Another
point in this respect is that the Cx. quinquefasciatus colony we
used did not live for more than three generations beyond 30 C (Gnay
et al. 2010), posing a limit on the temperature range expansion
that can be used. Both fathers and their sons show the same range
of variation and there are no significant differences among the
pairs of fathers, sons, and fathers-and-sons at all temperatures
(Table 1). The interesting outcome is that the narrow-sense
heritability, which is the amount of additive genetic variation
that contributes to the phenotypic variation in a trait, follows
the temperature increase. For each different developmental
temperature there is a correspondingly different heritability
estimate and the heritability increases with increasing
temperatures. We have estimated the narrow-sense heritability as a
function of the regression of the size values of the sons on the
fathers values. The regression coefficients (b) should show the
same increase with increasing temperature (Table 2). This suggests
that the amount of causality association (as indicated by
regression coefficients, b) changes in a directional way. Hence,
there is no fixed heritability for size when the environment
changes. This result can be taken as the expression of the well
substantiated general observation that a change in environment in
which heritability is measured will ensue in different values. As
the quantitative trait in question is affected by many genes with
small independent allelic contributions, as expected from the
classical additive theory of quantitative genetics,
it may easily yield different trait values with environmental
change (Falconer and Mackay 1996). This is typical in many
laboratory results (Mackay 2001). However, because the organisms do
not live in isolation and do experience environmental variation
continuously in their lifetimes in nature, our findings may also
point to natural situations in which temperatures change
frequently. This would be the simplest corollary from our results,
supporting a general truth reflecting one of the many situations in
nature. What is remarkable is the increase in the genetic variation
(as expressed by h2). We suggest this increase may be due to a
change in the expression of the genetic variation for body size. We
have estimated the additive genetic variation in each case
(Falconer and Mackay 1996). If the putative genes affecting body
size contribute to the trait value equally and independently from
each other, some genes hidden because of the trade-offs for
physiological threshold reasons could be manifest in their effect
in response to temperature raise. That effect is well known and is
the result of the unleashing of cryptic genetic variation due to
the decanalization of the genetic variance for a trait (Gibson and
Dworkin 2004, Gibson 2009). This would be reflected in an
incremental raise in the expression of genetic variation, which
seems to be the case for our results across the increasing
temperature regime.
The other point, which is related to the temperature dependent
increase in genetic variation in our study, is that the change in
the genetic variation could be the result of non-negligible G x E
for body size. Indeed, this is the case here. We have made a plot
of reaction norm for h2 (Figure 2). This plot provides a clear
illustration of the presence of G x E for body size across the
temperature range. To assess quantitatively if G x E occurs, we
have performed cross-environment correlation analyses between the
phenotypic expressions (i.e., wing aspect ratio, WAR) of body size
of the sons raised at different temperatures for heritability
analysis. The idea was that if there were genotype-by-environment
interactions, correlations between environmental pairs would be
less than unity (Mackay and Anholt 2007). This is again the case;
all correlation coefficients are less than unity, stressing the
presence of G x E for body size. Overall, we suggest that the
additive genetic variation for body size can strongly respond to
temperature variation. Our findings may indicate very important
ecological aspects with respect to the distribution of Cx.
quinquefasciatus. The global phenomenon of warming is of central
importance in this respect. Our findings show that increases in
temperature can be reflected by an increase in genetic variance,
possibly by unleashing cryptic genetic variation. This increase is
of the body size, and body size in turn is determinative in
important fitness components such as developmental time and the
related overall survival. Along with a trade-off between the food
scarcity and larger sizes, small individuals may survive and
reproduce better when food is limited because they need less food
to sustain themselves (Dingle 1992, Blanckenhorn et al. 1994). This
may mean that temperature increases can trigger better adaptations
via smaller body sizes even when food is scarce in the changing
environment. This could be
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Vol.36,no.2 Journal of Vector Ecology 353
expected to create greater distribution through warming
environments. That the genetic variation can be greater for
increasing temperatures may have remarkable distribution effects.
Indeed, there is a trade-off between desiccation tolerance and body
size. The more tolerant individuals are, the smaller they are in
size (Alpert 2006). What is striking is that the higher amounts of
genetic variation in desiccation tolerance as measured by
narrow-sense heritability can be directly related to a wider
distribution. In a recent study, Kellerman et al. (2009) found
that, along with cold tolerance, the differences in distribution
between the specialist/narrowly distributed species and
generalist/widely distributed species of Drosophila are clearly
related to the amount of the genetic variation (narrow-sense
heritability) in desiccation tolerance. The more tolerant species
appear to have higher narrow-sense heritability and wider
distribution as generalists. Contrastingly, lower amounts of
narrow-sense heritability correspond to the lower desiccation
tolerance of the narrowly distributed specialist species (Kellerman
et al. 2009). The desiccation is a direct function of the increased
temperatures, with organisms having greater genetic variation in
desiccation tolerance. The increase of the expression of genetic
variation in response to the temperature increases we found in our
study may point to the potential of range expansion in Cx.
quinquefasciatus when environments become warmer.
In conclusion, we suggest that our study of the effect of
temperature change on the amount of genetic variation of body size
in Cx. quinquefasciatus can reflect the fitness variation in local
adaptive perspectives as well as the more important issue of
species distribution. We believe our results contribute to the
general explanations of adaptation in the context of global
warming. A next step would be to work out the genomic expression
profiles in response to temperature shifts in Cx. quinquefasciatus
to find the candidate genes affecting body size in relation to
their pleiotropies with respect to the correlated traits. But, as a
first approximation, we also believe in the still invaluable
quality of the classical quantitative genetic assessment of genetic
variation as narrow-sense heritability (h2) estimates for the
traits correlated with body size, such as developmental time and
desiccation resistance. An alternative and a good start, therefore,
would be to design experiments of heritability for such correlated
traits. The overall scheme would be valid and worthwhile for other
species of mosquitoes.
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