ORIGINAL RESEARCH
published: 12 September 2016
doi: 10.3389/fphys.2016.00401
The Environmental Plasticity of
Diverse Body Color Caused by
Extremely Long Photoperiods and
High Temperature in Saccharosydne
procerus (Homoptera: Delphacidae)
Haichen Yin 1 , Qihao Shi 1 , Muhammad Shakeel 1 , Jing Kuang 2 and Jianhong Li 1*
1
2
Edited by:
Subhash Rajpurohit,
University of Pennsylvania, USA
Reviewed by:
Fei Li,
Nanjing Agricultural University, China
Guo-Hua Huang,
Hunan Agricultural University, China
*Correspondence:
Jianhong Li
jianhl@mail.hzau.edu.cn
Specialty section:
This article was submitted to
Integrative Physiology,
a section of the journal
Frontiers in Physiology
Received: 29 February 2016
Accepted: 29 August 2016
Published: 12 September 2016
Citation:
Yin H, Shi Q, Shakeel M, Kuang J and
Li J (2016) The Environmental
Plasticity of Diverse Body Color
Caused by Extremely Long
Photoperiods and High Temperature
in Saccharosydne procerus
(Homoptera: Delphacidae).
Front. Physiol. 7:401.
doi: 10.3389/fphys.2016.00401
Frontiers in Physiology | www.frontiersin.org
Department of Plant Protection, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China,
Wuhan Vegetable Research Institute, Wuhan, China
Melanization reflects not only body color variation but also environmental plasticity. It is a
strategy that helps insects adapt to environmental change. Different color morphs may
have distinct life history traits, e.g., development time, growth rate, and body weight.
The green slender planthopper Saccharosydne procerus (Matsumura) is the main pest
of water bamboo (Zizania latifolia). This insect has two color morphs. The present study
explored the influence of photoperiod and its interaction with temperature in nymph stage
on adult melanism. Additionally, the longevity, fecundity, mating rate, and hatching rate of
S. procerus were examined to determine whether the fitness of the insect was influenced
by melanism under different temperature and photoperiod. The results showed that a
greater number of melanic morphs occurred if the photoperiod was extremely long. A
two-factor ANOVA showed that temperature and photoperiod both have a significant
influence on melanism. The percentages of variation explained by these factors were
45.53 and 48.71%, respectively. Moreover, melanic morphs had greater advantages than
non-melanic morphs under an environmental regime of high temperatures and a long
photoperiod, whereas non-melanic morphs were better adapted to cold temperatures
and a short photoperiod. These results cannot be explained by the thermal melanism
hypothesis. Thus, it may be unavailable to seek to explain melanism in terms of only one
hypothesis.
Keywords: green slender planthopper, life traits, melanization, plasticity, thermal melanism hypothesis
INTRODUCTION
The green slender planthopper Saccharosydne procerus (Matsumura) is the principal pest of water
bamboo (Zizania latifolia) and has also been shown to damage rice (Oryza sativa) in some East
Asian countries such as China and Vietnam. Some green slender planthoppers have a black spot
on the terminus of the forewing (Figure 1). These phenotypes represent the melanic morph of
the species (Yin et al., 2015). The black spot appears after emergence. Melanism in this species
does not change over the adult stage. Previous studies have shown that the proportion of adult
melanic morphs is influenced by the environmental temperature in the nymph stage. Under
high- temperature conditions, there are more melanic morphs (Mao, 2008; Kuang, 2012). This
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The Environmental Plasticity of Saccharosydne procerus
warmer habitats (Rajpurohit et al., 2008). These studies indicate
a complex effect of the environmental temperature on insect
melanism. In view of the complicated mechanism involved, the
TMH must not be the only explanation of melanism. Therefore, it
cannot provide a universal explanation for melanism (Wittkopp
et al., 2003).
Although much information about melanism in insects is
available to date, little is known about melanism in aquatic
vegetable pests such as S. procerus. Melanism in this specie
has been shown to be influenced by temperature. Its pattern
is opposite to the one predicted by the TMH (Mao, 2008;
Kuang, 2012). Hence, it is interesting to study the variation of
the environmental plasticity caused by melanism. Additionally,
we suggest that it would be worthwhile to study the influence
of photoperiod on melanism and the relationship between the
effects of temperature and photoperiod on melanism.
The effect of photoperiod on melanism was investigated
in this study. A two-factor ANOVA was employed to analyze
the relationship between the influences of temperature and
photoperiod on melanism. Moreover, the longevity, fecundity,
mating rate, and hatching rate of S. procerus were examined
to investigate whether the fitness of the insect in the studied
environments was influenced by melanism under variations
in temperature and photoperiod. In particular, as melanism
persists in the adult stage, we predicted that some life history
traits of the two morphs would show contrasting differences in
the adult stage. The variation in the proportion of melanism
may be caused by differences in the adaptations of the two
morphs, or melanism may be a way for S. procerus to
adjust in the environmental changes. Because S. procerus faces
pressure caused by simultaneous variations in temperature and
photoperiod in the natural environment, we consider it of
interest to explore the relative significance of these two factors for
melanism.
FIGURE 1 | The non-melanic and melanic Saccharosydne procerus. (A)
Non-melanic morph and (B) Melanic morph. Figure adapted from Yin et al.
(2015).
pattern contradicts the thermal melanism hypothesis (TMH).
This hypothesis predicts that dark individuals with low skin
reflectance will heat faster than lighter individuals so that melanic
morphs will have an advantage in cool climates and under a short
photoperiod (Clusella-Trullas et al., 2008).
To date, the TMH has been confirmed by a large number
of studies. For example, cuticle melanism of the ground cricket
Allonemobius socius had a positive association with season
length (Fedorka et al., 2013); body melanization of Drosophila
melanogaster showed significant correlations with temperature,
and individuals fed in cool conditions were darker (Parkash et al.,
2010); additionally, the frequency of the melanic two-spotted
ladybird Adalia bipunctata decreased as a result of an increase in
local ambient spring temperatures (de Jong and Brakefield, 1998).
Melanization not only reflects body color variation, but also
environmental plasticity (Karlsson and Forsman, 2010); it is a
strategy used by insects to adapt to the environmental alterations
(van’t Hof et al., 2011). According to the TMH, dark individuals
absorb heat faster than lighter ones (Clusella-Trullas et al.,
2008). Hence, different body colors lead to variation in body
temperatures, and such variation may affect many life history
traits (Su et al., 2013), e.g., development time, growth rate, and
body weight (Cotter et al., 2008; Ma et al., 2008).
Although the TMH is widely accepted, we can still identify
some counterexamples. Female Tetranychus spider mites did
not show dark cuticular pigmentation when exposed to shortday and low-temperature conditions (Ito et al., 2013). In some
cases, melanic morphs were observed in some tropical areas and
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MATERIALS AND METHODS
Rearing of S. procerus
In this study, S. procerus were reared on water bamboo grown
in the greenhouse of Huazhong Agriculture University, Wuhan
(N30◦ 28′ , E114◦ 21′ ), China. To provide living conditions similar
to the natural habitat, the greenhouse was only covered by a gauze
net. The S. procerus in the present study were not exposed to any
pesticides. Hence, they did not face any selection pressure from
pesticides.
The Effect of Photoperiod on Melanism
Leaves of water bamboo with spawning marks were collected in
the greenhouse. These eggs were placed in an artificial climate
box at 26◦ C with L:D 16:8 h photoperiod. Four photoperiod
treatments (8:16, 12:12, 16:8, 20:4; 26◦ C) were employed to
explore the effect of photoperiod on melanism. Five nymphs
were placed on one water bamboo leaf in a glass tube (14 ×
1.5 cm). Each replicate contained 25 nymphs and each treatment
contained four replicates. Therefore, 100 individuals were used in
one treatment.
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The Contribution of Photoperiod and
Temperature to Variations in Melanism
To compare the relative influence of photoperiod and
temperature on melanism, four treatments (20:4, 30◦ C; 20:4,
22◦ C; 8:16, 30◦ C; 8:16, 22◦ C) were employed. The egg collection
and rearing methods used were stated above.
A two-factor ANOVA showed that temperature and photoperiod
both have significant influences on melanism (P < 0.01). The
percentages of variation in melanism explained by photoperiod
and temperature were 45.53% and 48.71%, respectively. The
interaction between photoperiod and temperature explained
3.57% of the total variation in melanism (Figure 3).
Observation of Life Traits
Adult Longevity
Under 22◦ C, the male adult longevity of two color morphs was
11.3 ± 2.54 (melanic morphs) and 18.8 ± 1.79 (non-melanic
morphs), respectively, while, when the temperature increased to
Water bamboo leaves with spawning marks were gathered from
the field to facilitate the collection of eggs of green slender
planthoppers. These eggs were placed in an artificial climate box
at 26◦ C and L:D = 16:8 photoperiod to feed for one generation.
A pair of melanic adults or non-melanic adults was placed
in one glass tube (14 × 1.5 cm) with one water bamboo leaf.
Each experimental tube received a selected combination of
temperature and photoperiod; three temperatures (22◦ C, 26◦ C,
and 30◦ C, all at L:D = 16:8 photoperiod) and three photoperiods
(12:12, 16:8, and 20:4; all at 26◦ C) were used in this experiment.
The experiment was performed to compare selected life history
traits of adults, namely, adult longevity, fecundity, mating rate,
hatching rate, pre-oviposition period, and egg stage duration. All
the data were recorded daily. The leaves were changed once a
day, and 100 melanic adults and 100 non-melanic adults were
employed for each treatment. The rationale for selecting these
temperatures was that under these treatments, the melanism
proportion was found to differ significantly; moreover, a previous
study showed that these conditions were suitable for S. procerus
(Kuang, 2012).
Statistical Analysis
FIGURE 2 | The proportion of melanism (mean ± SD) under different
photoperiods. The proportion of melanism increased when the light period
become longer. The proportion of melanism under 16:08 was significantly
higher than that under 12:12 (P = 0.0341) or 8:16 (P = 0.0279). The same
letter represent there is no significant differences in statistics. The capital letters
represent the level of 1%, the lower-case letters represent the level of 5%.
In the present study, one-way ANOVA and pairwise assessment
using the Multiple Range Test were applied to analyze the effect
of photoperiod on melanism and the influence of the studied
factors on life history traits. A two-factor ANOVA was employed
to analyze the contributions of photoperiod and temperature to
variation in melanism. All analyses were conducted with SPSS
Statistics 17.0.
RESULTS
The Effect of Photoperiod on Melanism
The proportion of melanic morphs increased from 0.56 ± 0.03
under short photoperiod (L:D = 8:16) to 0.7 ± 0.04 under
long photoperiod (L:D = 20:04) (Figure 2). The results showed
that long photoperiod is beneficial to improve the number of
melanic morphs. The analysis of one-way ANOVA showed that
the proportion of melanism under 16:08 was significantly higher
than that under 12:12 (P = 0.0341) and 8:16 (P = 0.0279).
The differences between the melanism proportions under 20:04
and 16:08 were not significant (P > 0.05). The proportion of
melanism under 12:12 did not differ significantly from that under
8:16 (P > 0.05).
FIGURE 3 | The effect of temperature, photoperiod, and their
interaction on the proportion of melanism (mean ± SD). A two-factor
ANOVA showed that temperature and photoperiod both have a significant
influence on melanism (P < 0.01). The proportions of total variance explained
by photoperiod and temperature were 45.53 and 48.71%, respectively. The
same letter represent there is no significant differences in statistics. The capital
letters represent the level of 1%, the lower-case letters represent the level
of 5%.
The Contributions of Photoperiod and
Temperature to Variations in Melanism
Under high temperature and extremely long photoperiod (30◦ C,
L:D = 20:04) the melanism proportion was 0.61 ± 0.01 while this
proportion decreased to 0.25 ± 0.03 under 22◦ C at L:D = 8:16.
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30◦ C, it was 13.8 ± 0.84 (melanic morphs) and 10.2 ± 3.03
(non-melanic morphs), respectively. The male adult longevity
of two morphs varied from 5.4 ± 1.34 (melanic morphs) and
13.8 ± 1.92 (non-melanic morphs) under 12:12 to 14.7 ± 1.51
(melanic morphs) and 10.0 ± 1.84 (non-melanic morphs) under
20:04.
Similarly under 22◦ C the female adult longevity of two color
morphs was respectively 10.0 ± 1.06 (melanic morphs) and
16.2 ± 2.17 (non-melanic morphs), while when temperature
increased to 30◦ C, it was 12.0 ± 1.87 (melanic morphs) and 8.8
± 0.45 (non-melanic morphs), respectively. With the change
of photoperiod, the female adult longevity of two morphs also
changed from 5.25 ± 0.90 (melanic morphs) and 15.4 ± 1.52
(non-melanic morphs) under 12:12 to 14.1 ± 0.89 (melanic
morphs) and 8.45 ± 1.23 (non-melanic morphs) under 20:04.
One-way ANOVA showed that under all temperature and
photoperiod treatments, there were no significant differences
between the longevity of male adults and that of female adults
(P > 0.05). The longevity of non-melanic male and female
adults was significantly longer than that of melanic male adults
(P = 0.0006) and female adults (P = 0.0004) at 22◦ C. At 26◦ C,
the longevity of non-melanic adults did not differ significantly
from that of melanic morphs (P > 0.05). The longevity of
melanic male and female adults was significantly longer than
that of non-melanic male adults (P = 0.0337) and female adults
(P = 0.0059) at 30◦ C.
Under the 12:12 photoperiod, non-melanic males and females
had a greater longevity than that of melanic males (P < 0.0001)
and females (P < 0.0001). Melanic males and females had a
longer longevity than non-melanic males (P = 0.0013) and
females (P < 0.0001) under the 20:04 photoperiod. There were
no significant differences among the treatment groups under the
16:08 photoperiod (P > 0.05) (Figure 4).
Fecundity per Female
The fecundity per female of melanic morphs varied from 27.0
± 4.00 under 22◦ C and 48.4 ± 5.58 under 12:12 to 99.0 ±
21.84 under 30◦ C and 46.7 ± 1.10 under 20:04. For non-melanic
morphs, fecundity per female changed from 72.0 ± 16.386
(22◦ C), 80.9 ± 16.98 (12:12) to 68.2 ± 5.67 (30◦ C), 35.5 ± 7.07
(20:04), respectively.
One-way ANOVA showed that the fecundity per female of
melanic morphs was markedly higher than that of non-melanic
morphs at 30◦ C (P = 0.0158) and 20:04 (P = 0.0081), and lower
than that of non-melanic morphs at 22◦ C (P = 0.0003) and 12:12
(P = 0.0036). There were no statistically significant differences
FIGURE 4 | Adult longevity (mean ± SD) of S. procerus. (A) Male adult longevity at different temperatures. (B) Female adult longevity at different temperatures.
(C) Male adult longevity under different photoperiods. (D) Female adult longevity under different photoperiods. Under all temperature and photoperiod treatments,
there were no significant differences between the longevity of male adults and that of female adults (P > 0.05). The longevity of melanic adults was significantly longer
than that of non-melanic adults at 30◦ C and 20:04 but shorter than that of non-melanic adults at 22◦ C and 12:12 (P < 0.01). The same letter represent there is no
significant differences in statistics. The capital letters represent the level of 1%, the lower-case letters represent the level of 5%.
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FIGURE 5 | The fecundity per female (mean ± SD) of S. procerus. (A) The fecundity per female at different temperatures. (B) The fecundity per female under
different photoperiods. The fecundity of melanic females was significantly higher than that of non-melanic females at 30◦ C and 20:04. It was lower than that of
non-melanic females at 22◦ C and 12:12 (P < 0.01). The same letter represent there is no significant differences in statistics. The capital letters represent the level of
1%, the lower-case letters represent the level of 5%.
between the two morphs at 26◦ C or under 16:08 (P > 0.05)
(Figure 5).
differences between the two morphs at 26◦ C or under 16:08.
(P > 0.05) (Figure 6).
Mating Rate
Hatching Rate
If a female adult produced no offspring, that female was
considered as failed to mate. When the temperature increased,
the mating rate of melanic morphs varied from (66.0 ± 5.48)%
to (60.0 ± 7.07)%, similarly, it was (92.0 ± 8.37)% under 22◦ C
and decreased to (44.0 ± 5.48)% under 30◦ C for non-melanic
morphs. Under 12:12, it was (52.502 ± 2.28)% (melanic morphs)
and (84.446 ± 6.09)% (non-melanic morphs), when the daytime
became longer it was (95.0 ± 6.09)% (melanic morphs) and (70.0
± 6.85)% (non-melanic morphs), respectively, under 20:04.
One-way ANOVA showed that the mating rate of melanic
morphs was significantly higher than that of non-melanic
morphs at 30◦ C (P = 0.0039) and under 20:04 (P = 0.0002) and
lower than that of non-melanic morphs at 22◦ C (P = 0.0004) and
under 12:12 (P < 0.0001). There were no statistically significant
When the temperature and daytime increased, the hatching
rate of eggs produced by melanic morphs increased from
(54.526 ± 10.18)% and (46.778 ± 7.44)% to (79.464 ±
7.61)% and (78.037 ± 4.42)%, while it decreased from (85.45
± 4.54)% and (71.689 ± 4.97)% to (56.618 ± 8.95)% and
(46.416 ± 5.79)% for non-melanic morphs, respectively.
One-way ANOVA showed that eggs produced by non-melanic
adults had a significantly higher hatching rate than that of eggs
produced by melanic adults at 22◦ C (P = 0.0003) and under
12:12 (P = 0.0003). The hatching rate of eggs produced by
melanic adults was significantly higher than that of eggs produced
by non-melanic adults at 30◦ C (P = 0.0025) and under 20:04
(P < 0.0001). No significant differences between two morphs
were found at 26◦ C or under 16:08 (P > 0.05) (Figure 7).
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FIGURE 6 | Mating rate (%) (mean ± SD) of S. procerus. (A) Mating rate (%) at different temperatures. (B) Mating rate (%) under different photoperiods. The
mating rate of melanic morphs was significantly higher than that of non-melanic adults under 30◦ C and 20:04. It was lower than that of non-melanic adults at 22◦ C
and 12:12 (P < 0.01). The same letter represent there is no significant differences in statistics. The capital letters represent the level of 1%, the lower-case letters
represent the level of 5%.
Preoviposition Period and Egg Period
DISCUSSION
When the temperature increased from 22◦ C to 30◦ C, the preoviposition of melanic and non-melanic morphs varied from
(6.6 ± 1.5477) d and (5.0 ± 1.7070) d to (4.0 ± 0.7071) d and
(3.8 ± 0.4472). Egg period of melanic and non-melanic morphs
varied from (15.0 ± 0.7701) d and (16.4 ± 1.3416) d to (10.2
± 2.2804) d and (11.8 ± 1.7889) d. Pre-oviposition and egg
period of two morphs both shortened when the temperature
increased.
When the photoperiod increased from 12:12 to 20:04, the preoviposition of melanic and non-melanic morphs varied from (5.2
± 0.7583) d and (5.0 ± 1.0000) d to (5.0 ± 1.5811) d and (5.1 ±
0.4472) d. Egg period of melanic and non-melanic morphs varied
from (11.8 ± 1.3038) d and (10.7 ± 0.6708) d to (12.0 ± 0.7071)
d and (11.1 ± 0.7416) d. Pre-oviposition and egg period of two
morphs did not varied significantly under different photoperiod.
One-way ANOVA showed that the preoviposition period and egg
period had no significant differences between the two morphs
(P > 0.05).
A previous study has shown that the proportion of melanism in
S. procerus increased under higher temperature in the laboratory.
This finding was also obtained in a field study, previous field
investigation in four primary water bamboo producing areas
showed that the proportion of melanic morphs was highest in the
areas that had highest mean temperature, field investigations in
Wuhan (N30◦ 28′ and E114◦ 21′ ), China from June to October 2012
also proved that high temperature improve the melanic proportion
(Yin et al., 2015). In the present study, our data showed that
photoperiod also had marked effects on melanism in S. procerus
besides temperature. Notably, the photoperiod that was found to
have a statistically significant effect on the proportion of melanism
was an extreme case. Accordingly, we speculated that the influence
of photoperiod might be not as strong as that of temperature.
However, this speculation was not supported by a two-factor
ANOVA. This analysis found that the percentages of variation in
melanism explained by photoperiod and temperature were 45.53
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FIGURE 7 | Hatching rate (%) (mean ± SD) of S. procerus. (A) Hatching rate at different temperatures. (B) Hatching rate under different photoperiods. The
hatching rate of melanic morphs was significantly higher than that of non-melanic adults at 30◦ C and 20:04. It was lower than that of non-melanic adults at 22◦ C and
12:12 (P < 0.01). The same letter represent there is no significant differences in statistics. The capital letters represent the level of 1%, the lower-case letters represent
the level of 5%.
investment will influence body color (Mills, 2012). Similarly, we
speculated that the body color of S. procerus may change in the
same way. According to previous study, increased temperature is
usually associated with the increase in infectious diseases (Roulin,
2014). Hence, melanic morphs of S. procerus appeared, which
may be due to the higher PO activity and melanin synthesis
caused by greater infectious risk under high temperature (Wilson
et al., 2001; Eleftherianos and Revenis, 2011). Additionally, the
UV-absorbing properties of melanin are believed to be involved
in protecting the organism from UV-induced DNA damage (Li
et al., 2015). Indeed, a previous study showed that UV-exposed
animals usually had a higher melanin content and became
darker (Debecker et al., 2015). Therefore, we speculated that the
melanism of S. procerus induced by extremely long photoperiods
serves to facilitate UV protection. Moreover, we infer that the
multiple function of melanin may not only change the body color
of S. procerus, but also the environmental fitness.
and 48.71% respectively. Nevertheless, given that this photoperiod
used in our laboratory study does not actually occur in the field,
so the variation in the proportion of melanism in S. procerus in
the principal areas of water bamboo (Z. latifolia) production in
China should still be explained by the effect of temperature.
Several previous studies showed that the host-pathogen
interaction can be influenced by the thermal environment (Cotter
et al., 2008; Catalán et al., 2012). When a pathogen binds to
a pattern recognition receptor, the prophenoloxidase-activating
proteinase (PAP) will convert pro-phenoloxidase (PPO) to
phenoloxidase (PO) (Yu et al., 2003). After this conversion, PO
is involved in the synthesis of melanin with the oxidation of LDopa or dopamine, and this process contributes to both pathogen
defense and melanism (Fedorka et al., 2013). When faced with
a greater risk of infection, individuals will invest more in the
immune system (Wilson and Reeson, 1998). Due to the close
connection between melanization and immune response, this
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The Environmental Plasticity of Saccharosydne procerus
conditions (Ahnesjö and Forsman, 2006). Another example is
the hypothesis that dark-colored damselfly larvae will normally
be cryptic in their environment but will have a high risk of
being preyed upon when observed against a white background
(Johansson and Nilsson-Örtman, 2013).
The studies cited above identified potential selective
disadvantages affecting melanic morphs under certain
conditions. For this reason, melanism can at times be a cue
for mate choice because it signals environment-dependent
fitness to potential mates. For example, females of Harmonia
axyridis prefer succinea-form males to melanic males in the
spring generation due to the disadvantages experienced by
melanic morphs during the summer (Su et al., 2013). Similarly,
we infer that female S. procerus will also have their own mating
preferences based on fitness variation in different environments
although the melanic pattern found in the species is opposite to
that expected from the THM. We consider that this preference
may influence the rate of successful mating in S. procerus under
different temperatures and photoperiods.
In summary, we found that photoperiod, in addition to
temperature, is an environmental factor that influences melanism
in S. procerus. Additionally, the adult longevity, fecundity, mating
rate, and hatching rate of S. procerus were examined in the
present study. Our results suggest that melanic morphs enjoy
advantages in hot environments and under long photoperiods,
whereas non-melanic morphs can adapt more successfully to
low temperatures and short photoperiods. These results did
not support the TMH. In view of the demonstrated differences
in fitness between the two studied color morphs, we infer
that the frequency of melanic morphs will increase as a
result of continued increase in temperature associated with
future global warming. The melanism of S. procerus appears
in the adult stage but is a response to the environmental
pressure experienced by the nymph. However, the mechanisms
by which stressors in the nymphal or larval stage affect the
adult stage remain unclear (Debecker et al., 2015). Additionally,
it may be worthwhile to explore the genetic regulation of
melanism to clarify the effect of heredity on the body color of
S. procerus.
In this study, differences between the life history traits of the
two studied morphs under different conditions were compared
to explore the influence of melanism on the fitness of S. procerus.
We found that melanic morphs enjoyed a greater advantage than
non-melanic morphs in a hot environment and under extremely
long photoperiod, whereas, non-melanic morphs were better
adapted to cold conditions and relatively short photoperiods.
These results showed that the melanism of S. procerus is
expressed not only as variation in body color but also in fitness
differences in the studied environments. Given that melanism
can be induced in hot environments and under extremely long
photoperiod, we think that melanism may be a strategy by which
S. procerus adapts to environmental alterations. However, the
thermal plasticity of S. procerus cannot be explained by the
TMH. Insects face complex selection pressures. Hence, it may be
inadvisable to explain melanism in terms of only one hypothesis
(Wilson et al., 2001). Different selection pressures may result in
patterns that are not consistent with the TMH.
Several previous studies have shown that the TMH can fail
to explain relationships between melanism and environmental
adaptations. In some cases, melanic morphs could be induced
at relatively high temperatures or under a high level of incident
radiation and were advantageous under warm conditions
(Välimäki et al., 2015). The melanism of those species may arise
from an interaction between thermal selection and other selective
factors, especially over a wide geographical scale (Brakefield,
1985).
According to previous studies, the immunocompetence of
darker individuals is usually greater than that of lighter ones
(Armitage and Siva-Jothy, 2005). For example, the melanic
morphs of Spodoptera exempta showed a significantly higher
resistance to baculovirus than non-melanic morphs (Reeson
et al., 1998), and melanic Tenebrio molitor showed lower
mortality when exposed to a generalist entomopathogenic fungus
(Barnes and Siva-Jothy, 2000). Additionally, melanic morphs of
Ephestia kuhuiella were better able to inhibit the oviposition
and larval development of parasitic wasps (Verhoog et al.,
1996). Therefore, as we discussed above, we infer that the
fitness advantages of melanic morphs at high temperatures
may be explained by increased investment in melanin-based
immunocompetence in the face of the greater risk of infection
in a hotter environment (Roulin, 2014).
Although melanic morphs have multiple advantages,
disadvantages still exist when the selection pressure changes.
Melanin-based coloration is costly in terms of energy and other
resources because it requires investment in production and
maintenance (Roulin, 2015). A trade-off is needed between
melanin-based coloration and other biological processes
(Sheldon and Verhulst, 1996). This allocation problem may be
solved by a distinctive pattern of investment in diverse aspects
of body conditions in different color morphs that may result in
different physiology or behavior. Thus, one morph is adapted to
a given environmental condition but may exhibit maladaptation
if this given environment is altered (Roulin, 2015). Hence,
in the absence of certain selective factors, melanic morphs
will have some disadvantages. For instance, darker morphs of
pygmy grasshoppers (Orthoptera: Tetrigidae) usually select cool
habitats due to the risk of overheating in hot environmental
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ETHICS STATEMENT
Our work conforms to the legal requirements of the country in
which it was carried out.
AUTHOR CONTRIBUTIONS
HY and JL: conception and design of research; HY and QS:
performed experiments; HY: analyzed data; HY, QS, MS, JK, and
JL: interpreted results of experiments; HY, MS: prepared figures;
HY, MS: drafted manuscript; HY, MS, and JL: edited and revised
manuscript; HY, QS, MS, JK, and JL: approved final version of
manuscript.
ACKNOWLEDGMENTS
This work was supported by the National Key Technology R&D
Program of China (No. 2012BAD27B02), and the Fundamental
Research Funds for the Central Universities (No. 2014PY036).
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Yin et al.
The Environmental Plasticity of Saccharosydne procerus
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2016 Yin, Shi, Shakeel, Kuang and Li. This is an open-access article
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September 2016 | Volume 7 | Article 401