Content uploaded by Dao-Hong Zhu
Author content
All content in this area was uploaded by Dao-Hong Zhu on Nov 07, 2014
Content may be subject to copyright.
1 23
Evolutionary Biology
Evolutionary Biology
ISSN 0071-3260
Volume 41
Number 3
Evol Biol (2014) 41:397-403
DOI 10.1007/s11692-014-9272-9
Critical Flight Time for Switch from Flight
to Reproduction in the Wing Dimorphic
Cricket Velarifictorus aspersus
Yang Zeng, Dao-Hong Zhu & Lü-Quan
Zhao
1 23
Your article is protected by copyright and all
rights are held exclusively by Springer Science
+Business Media New York. This e-offprint is
for personal use only and shall not be self-
archived in electronic repositories. If you wish
to self-archive your article, please use the
accepted manuscript version for posting on
your own website. You may further deposit
the accepted manuscript version in any
repository, provided it is only made publicly
available 12 months after official publication
or later and provided acknowledgement is
given to the original source of publication
and a link is inserted to the published article
on Springer's website. The link must be
accompanied by the following text: "The final
publication is available at link.springer.com”.
RESEARCH ARTICLE
Critical Flight Time for Switch from Flight to Reproduction
in the Wing Dimorphic Cricket Velarifictorus aspersus
Yang Zeng •Dao-Hong Zhu •Lu
¨-Quan Zhao
Received: 2 June 2013 / Accepted: 6 February 2014 / Published online: 18 February 2014
ÓSpringer Science+Business Media New York 2014
Abstract Flight dimorphism has been considered to
result from a balance of costs and benefits between flight
capability and reproduction. The validity of the hypothesis,
however, has been challenged recently. In this study, we
examined the effect of flight time on trade-off between
flight capability and reproductive development in Velarif-
ictorus aspersus and we found that flight of 5 min did not
promote reproductive development of long-winged (LW)
adults, but flight of 30, 60, or 120 min could promote
reproductive development both in female and male crick-
ets. The results indicate that flight time may serve as a
signal for LW V. aspersus to switch from migration to
reproduction, and trade-off between flight ability and
reproduction may be attenuated when flight time reaches a
critical threshold. In addition, rapid reproductive develop-
ment occurred before dealation when LW insects were
allowed to fly for 30 min, which indicates that flight may
influence reproductive development directly. Food con-
sumption of short-winged adults was significantly higher
than that of unflown LW adults or LW adults with 5 min
flight, but similar to that of LW adults with 30, 60, or
120 min flight, suggesting that difference of reproductive
development may be positively correlated with their food
consumption.
Keywords Migration Reproductive development
Trade-off Dealation Food consumption
Introduction
Migration is a life history trait that plays an important role in
insect population maintenance and evolution (Jiang et al.
2010). The behavior may cost a large amount of energy, thus
reducing energy investment in other life history traits.
Trade-off between flight capability and reproduction has
been observed in many insect taxa, particularly from studies
of wing-dimorphic field crickets (Harrison 1980;Roff1986;
Zera and Denno 1997). For flight capable insects, the
females usually have prolonged pre-oviposition period and
decreased egg production in early adulthood (Dingle and
Arora 1973;WaltersandDixon1983;Roff1984;Zera1984;
Mole and Zera 1994) while the males have smaller acces-
sory gland and invest less energy in female attracting
behaviors (Crnokrak and Roff 2000; Guerra and Pollack
2007;Zengetal.2012). However, most of these studies
have been conducted without considering effect of flight
behavior. In some wing monomorphic insect species such as
Melanoplus sanguinipes and Gryllus bimaculatus (McA-
nelly and Rankin 1986; Dyakonova and Krushinsky 2008),
flight behavior increased reproductive output. By contrast,
Roff (1977) has found that flight reduces egg production of
Drosophila melanogaster. Fecundity of winged female
Aphis glycines engaged in [0.5 km long flights are signifi-
cantly lower than those of \0.5 km individuals (Jiang et al.
2010). In a wing dimorphic cricket species Gryllus texensis,
a short bout of flight eliminates trade-off between flight
capability and reproduction (Guerra and Pollack 2009;Gu-
erra (2011)) suggested that the trade-off may be under- or
overestimated and factors like flight muscle status, flight
behavior and environmental conditions may influence the
expression of this trade-off. But for another wing dimorphic
cricket species Gryllus rubens, flight does not have an effect
on this trade-off (Zera and Rankin 1989).
Y. Zeng D.-H. Zhu (&)L.-Q. Zhao
Laboratory of Insect Behavior and Evolutionary Ecology,
Central South University of Forestry and Technology,
Changsha 410004, Hunan, China
e-mail: daohongzhu@yeah.net
123
Evol Biol (2014) 41:397–403
DOI 10.1007/s11692-014-9272-9
Author's personal copy
The negative association between flight apparatus and
reproduction is often considered to be an adaptation that
permits the differential allocation of limited resources to either
flight muscle growth and maintenance or egg production in
alternate morphs (Harrison 1980; Penner 1985; Roff 1986).
This is based on the assumption that resources are limited
within the organism. Mole and Zera (1993) have investigated
nutritional indices of long-winged (LW) and short-winged
(SW) females in G. rubens, and found that the LW female eat
as much food as the SW females, but they allocate assimilated
nutrients in maintenance of functional flight muscles while the
SW females may devote them in ovarian tissue, suggesting
that differential allocation of resources underlies the dispersal-
reproduction trade-off. But for Modicogryllus confirmatus,
SW females eat significantly more food than the LW females,
which indicates that the elevated fecundity of the SW morph
may be due to increased food consumption over thatin the LW
morph (Tanaka 1993). In another wing dimorphic cricket
Gryllus firmus, LW females consume more food than SW
females (Mole and Zera 1994).
The cricket species Velarifictorus aspersus displays dis-
tinct wing dimorphism. LW females have longer preoviposi-
tion period and less fecundity than the SW females, and LW
males have smaller accessory gland and produce smaller
spermatophore than the SW males (Zeng et al. 2012). In this
study, tethered LW adults were allowed to fly for various
length of time and were examined for reproductive develop-
ment in order to test whether flight behavior influence
expression of this trade-off. In addition, data on food con-
sumption of these adults were collected over a period of 48 h
to test whether this trade-off is related with food consumption.
Materials and Methods
Experimental crickets V. aspersus were obtained from an
established laboratory colony that originated from a popula-
tion collected in Hainan Province, China. Crikets were reared
with ad libitum access to food and water under LD16: 8 h and
30 °C, as described in Zeng et al. (2012). LW crickets, aged
3 days after the last moult, were glued at the pronotum to a
wooden applicator stick and placed in front of a small fan to
promote flight. As control, 20 females or males were tethered,
but not allowed to fly. For doing this, crickets glued to a
wooden applicator stick and placed in front of a small fan for
60 min were provided with a wooden stick to rest on—
crickets would not fly when resting stick was provided.
Effect of Flight on Reproductive Development,
Dealation and Food Consumption in a Period of 48 h
A total of 20 LW females and males were tethered to fly for
5, 30, 60, or 120 min, respectively. They were subsequently
placed separately with pre-weighed fresh food. The
remaining food was removed at 48 h after treatment and
weighed after being dried at 100 °C for 24 h. The number of
the crickets that dealated hindwings naturally was counted.
All crickets were then dissected and their flight muscles and
reproductive organs were weighed using a digital scale
(0.0001 g). The flight muscles and reproductive organs were
dried at 100 °C for 24 h and weighed again. Unflown ani-
mals were examined at equivalent ages. A fresh weight
versus dry weight calibration curve was constructed to
estimate the dry weight of the food provided to the crickets.
Effect of Dealation on Reproductive Development
and Food Consumption
To examine effect of dealation on reproduction and food
consumption, hind wings of LW adults aged 3 days after
emergence were removed using forceps and were placed
separately with pre-weighed fresh food. Two days after
treatment, remaining food was removed and dry-weighed,
and their flight muscles and reproductive organs were
dissected out and weighed.
Effect of Flight on Reproductive Development in 24 h
To find out whether reproduction occurs before dealation,
20 LW females and 20 LW males aged 3 days after
emergence were each tethered to fly for 30 min. The
number of crickets that dealated hindwings was counted
24 h later and discarded, and those with intact hindwings
were disected, and their flight muscles and reproductive
organs were weighed. As a control, unflown LW females
and males of same age were also disected and their flight
muscles and reproductive organs were weighed.
Results
Effect of Flight on Trade-Off Between Flight
Capability and Reproduction
Long-winged-unflown insects had well-developed, pink
flight muscles, and SW ones had non-functional, white
flight muscles. LW-unflown females had smaller ovaries
and LW-unflown males had smaller accessory glands than
SW ones (Figs. 1,2). The color of the flight muscles of the
LW-flown crickets did not look very different from that of
LW-unflown crickets.
Fresh weight of flight muscles and ovary of LW females
with flight of 5 min were 10.74 ±0.69 and 3.69 ±0.32 mg,
respectively, and neither were significantly different from
that of unflown LW females (ANCOVA with body weight as
a covariate, fresh weight: F
1, 38
=1.79, P=0.18; dry
398 Evol Biol (2014) 41:397–403
123
Author's personal copy
weight: F
1, 38
=0.12, P=0.73). However, LW females
with flight of 30, 60, or 120 min had lighter flight muscles,
but larger ovaries than unflown LW females (P\0.001 in all
cases). Flight muscles of LW females with a flight of
C30 min were significantly heavier than that of SW females,
but no significant difference was observed in ovary weight
among them (Fig. 1). Like the females, there was no sig-
nificant difference of flight muscles, testis, or accessory gland
between LW-5 min males and LW-unflown males
(ANCOVA with body weight as a covariate, P[0.05).
Flight muscles of LW males with a flight of C30 min were
lighter than that of the control, but heavier than that of SW
males. Accessory glands of LW males with a flight of
0
10
20
30
40
50
60
xx
yyyyy
b
b
b
b
b
a
a
0
10
20
30
40
50
z
z
y
y
y
xx
c
c
b
b
b
a
a
Weight of ovaries (mg) Weight of flight muscles (mg)
(a)
(b)
LW-unflown
LW-5min flight
LW-30min flight
LW-60min flight
LW-120min flight
SW
DLW
Fig. 1 Effects of flight and dealation on flight muscle (a) and ovary
(b) development of female Velarifictorus aspersus in 48 h. Data are
mean ±SE, the same as below. Empty and solid bars indicate fresh weight
and dry weight, respectively. Different letters indicate a significant
difference between groups at 5 % level by ANCOVA with body weight as
a covariate. n =20 for each of the other experimental groups
0
3
6
9
12
15
yyy
y
x
x
y
b
b
b
b
b
a
a
0
5
10
15
20
x
x
x
x
x
x
x
a
a
a
a
a
a
a
0
10
20
30
40
50
z
z
y
y
y
x
x
c
c
b
b
b
a
a
Weight of flight muscles (mg)Weight of testis (mg)Weight of accessory gland (mg)
(a)
(b)
(c)
LW-5min flight
LW-unflown
LW-30min flight
LW-60min flight
LW-120min flight
SW
DLW
Fig. 2 Effects of flight and dealation on flight muscle (a), testis
(b) and accessory gland (c) development of male V. aspersus in 48 h.
Empty and solid bars indicate fresh weight and dry weight,
respectively. Different letters indicate a significant difference between
groups at 5 % level by ANCOVA with body weight as a covariate.
n=20 for each of the other experimental groups
Evol Biol (2014) 41:397–403 399
123
Author's personal copy
C30 min were larger than that of unflown LW males
(P\0.001), but similar with that of SW males (P[0.05).
No effect of flight on testis development was observed
(P[0.05 in all cases). The same result was obtained when
dry weight was analyzed (Fig. 2). This result suggests that a
short time of flight could not eliminate this trade-off in V.
aspersus, but a flight of more than 30 min could.
Effect of Dealation on Trade-Off Between Flight
Capability and Reproduction
Dealation had a significant effect on flight muscles and
reproductive development. Artificially dealated LW
(DLW) females had dramatically decreased flight muscle
mass, but significantly increased ovary mass than unflown
LW females (ANCOVA with body weight as a covari-
ate,P\0.001 in both cases). This effect was also observed
in DLW males. Flight muscles weight of DLW males were
significantly lower than that of unflown LW males (fresh
weight: F
1, 38
=149.16, P\0.001; dry weight: F
1, 38
=
86.15, P\0.001), but accessory gland weight of DLW
males were significantly higher than that of unflown LW
males (fresh weight: F
1, 38
=49.99, P\0.001; dry
weight: F
1, 38
=41.60, P\0.001) (Figs. 1,2).
Effect of Flight on Dealation
No unflown LW adult shed hind wings in 48 h. A flight of
5 min had no effect on dealation (Bonferroni-corrected v
2
test, a=0.005, P[0.05). However, almost all of LW
adults with flight of 30, 60, or 120 min shed their hind
wings, and dealation rate were all significantly higher than
that of the unflown LW (Bonferroni-corrected v
2
test,
a=0.005, P\0.001 in all cases) (Table 1).
Effect of Flight of 30 min on Reproductive
Development in Intact LW Adults
In order to test whether flight influences reproductive
development directly, or indirectly by affecting dealation, 20
LW females and males were each tethered to fly for 30 min,
and flight muscles and reproductive organs were dissected
from intact individuals after 24 h. Dealation rate was only
10 % for females and 15 % for males. Flight muscles of
intact LW-flown insects weighed similar to that of unflown
LW insects (ANCOVA with body weight as a covariate,
female: F
1, 36
=1.88, P=0.18; male: F
1, 35
=0.11,
P=0.74). However, ovary of the LW-flown females
weighed 18.46 ±0.82 mg, which was significantly heavier
than that of the unflown LW females (F
1, 36
=85.16,
P\0.001) (Fig. 3a). Accessory gland of the LW-flown
males with flight were also significantly heavier than that of
the unflown LW morph (ANCOVA with body weight as a
covariate, F
1, 35
=47.28, P\0.001) (Fig. 3b). These
results indicated that a long time flight could directly pro-
mote the reproductive development both in female and male
V. aspersus.
Table 1 Effect of flight on dealation of female and male Velarifict-
orus aspersus in 48 h
Treatment Dealation rate
of females (%)
Dealation rate
of males (%)
Sample
Unflown LW 0 0 20
LW-5 min flight 0 0 20
LW-30 min flight 100* 100* 20
LW-60 min flight 90* 100* 20
LW-120 min flight 100* 100* 20
Asterisk indicates dealation rate was significantly higher than that of
the unflown LW control (Bonferroni-corrected v
2
test, a=0.005)
0
10
20
30
40
50
Accessory
g
land
Testis
Fli
g
ht muscles
*
NS
NS
0
10
20
30
40
50
Flight muscles Ovary
*
NS
Fresh weight (mg)
(a)
(b)
Fig. 3 Effect of flight of 30 min on reproductive development in
intact LW female (a) and male (b)V. aspersus in 24 h. Empty and
solid bars indicate flown and unflown animals, respectively. NS
indicates no significant difference; asterisk indicates a significant
difference between groups, ANCOVA with body weight as a
covariate, P\0.05. n =18 for LW-flown females, 17 for LW-flown
males, and 20 for LW-unflown groups
400 Evol Biol (2014) 41:397–403
123
Author's personal copy
Food Consumption
Food consumption varied between females with different
flight treatments (ANOVA followed by Tukey-test,
F
6, 133
=120.36, P\0.001). Food consumption by LW-
unflown females was significantly lower than that of the
SW females (P\0.001). A flight of 5 min did not increase
food consumption of the LW females (P[0.05). How-
ever, food consumption of DLW, or LW females with
flight of 30, 60, or 120 min were all significantly higher
than that of the LW-unflown females (P\0.001 in all
cases) (Fig. 4).
Males consumed less food than females, but food con-
sumption also varied with treatment (ANOVA followed by
Tukey-test, F
6, 133
=69.59, P\0.001). SW males con-
sumed more food than LW-unflown or LW-5 min males
(P\0.001 in both cases), but no significant difference
existed between SW males and DLW males or LW males
with flight of 30, 60, or 120 min (P[0.05 in all cases)
(Fig. 4).
Discussion
A trade-off between flight capability and reproduction has
been demonstrated by numerous studies in migratory
insects and wing polymorphic insects, and the concept
plays an important role in understanding of the evolution of
life history traits. In this study, we found that a flight of
5 min did not influence this trade-off, but flight of C30 min
were able to attenuate this trade-off both in female and
male of the cricket species V. aspersus. Because almost all
of LW adults have partially histolyzed fight muscles at
48 h after a long time flight, we further investigate the
effect of a flight of 30 min on flight muscle and repro-
ductive development of intact LW insects to exclude
influence of flight muscle degeneration. The results showed
that flight influenced reproductive development directly. In
cricket G. texensis, a flight of 5 min is enough to promote
reproduction of the flight capable crickets (Guerra and
Pollack 2009), whereas a flight of more than 1 h was
unable to promote the reproductive output of the LW fe-
mals in G. rubens (Zera and Rankin 1989). Field obser-
vations were consistent with these findings—males of G.
texensis captured after having been observed flying in the
field have enhanced calling behavior relative to field cap-
tured SW males (Bertram 2007). In another wing dimor-
phic cricket species G. firmus, field-collected, flight-
capable females had smaller ovaries than short-winged
females or long-winged females with histolyzed muscles
(Zera et al. 2007). The results of these studies provide
conflicting evidences about whether flight can eliminate
this trade-off. If a critical flight time does exist in other
wing dimorphic insects and varies between different spe-
cies, one may expect to obtain different result when dif-
ferent insect species are used. To test the hypothesis,
further studies are needed in other wing dimorphic insects
and additional field observations of flight history of such
species.
Dealation occurs in a wide range of insect taxa,
including Zoraptera (Gurney 1938), Hymenoptera (Arnett
1985), Hemiptera (Andersen 1982), Blattodea (Mackerras
1970), Diptera (Colless and McAlpine 1970) and Orthop-
tera (Tanaka 1976; Roff 1984). This behavior can induce
degeneration of wing muscles and promote reproductive
development, and thus is selectively advantageous (Roff
1989; Tanaka 1991). In V. aspersus, we also found that
artificial dealation could induce degeneration of wing
muscles, and promote reproductive development and food
consumption. Natural dealation in Velarifictorus parvus
usually occurs after maximal ovipositing activity is
attained, suggesting that natural dealation is not the direct
cause for initiation of rapid egg production (Tanaka 1991).
In other insects, dealation also does not occur often in the
early stages of adult life when LW adults are not permitted
to fly (Roff 1984). Tanaka (1991) suggested that dealation
is probably a result rather than a causal factor in ending
migration. If dealation is a result of ending migration, what
would determine the timing of dealation. In this study, we
observed rapid reproductive development after a long time
of flight, and it occurred before dealation. The observation
is consistent with that of Guerra and Pollack (2009). These
0
10
20
30
40
xx
yyyyy
b
b
b
b
b
a
a
Food consumption (mg)
LW-unflown
LW-5min flight
LW-30min flight
LW-60min flight
LW-120min flight
SW
DLW
Fig. 4 Effects of flight and dealation on food consumption of female
(empty bars) and male (solid bars)V. aspersus in 48 h. Different
letters indicate a significant difference between groups at 5 % level
by ANOVA followed by Tukey-test. n =20 for each of experimental
groups
Evol Biol (2014) 41:397–403 401
123
Author's personal copy
authors observed, especially for the males, courtship
singing propensity of the LW males with flight was sig-
nificantly higher than that of the unflown LW males whe-
ther tested immediately or 10 h after flight (Guerra and
Pollack 2009). Based on these findings, we may infer that
long time flight above a threshold may induce rapid
reproductive development and termination of the migration
phase, resulting in natural dealation.
Tanaka (1993) has found food consumption of SW
females to be significantly higher than that of LW females
during first 5 days of the adult life in M. confirrmatus.
However, LW and SW female G. rubens consumed the
same amount of food during the first 2 weeks, and LW
female G. firmus consumed even more food than the SW
females during the first 12 days (Mole and Zera 1993,
1994). Obviously there exists an interspecific variation in
food consumption. Alternatively, the SW insects may con-
sume more food when they develop ovary quickly, but
reduce food consumption when the ovaries are fully devel-
oped. In contrast, the LW females initially consumed less
food when their ovaries develop slowly, but increase their
food consumption when their ovary developments acceler-
ate. If this is true, the average food consumption may not be
different between these two female wing morphs. Indeed,
the SW female G. firmus has developed ovaries quickly in
first 5 days, but the weight of their ovaries no longer
increased after that. For the LW females, ovaries developed
slowly during the first 7 days, but quickened after that (Mole
and Zera 1994). In V. aspersus, the SW adults consumed
more food than the LW adults that developed reproductive
organs slowly, but no significant difference existed between
SW adults and DLW adults or LW adults that developed
reproductive organs quickly. This result suggests that food
consumption may be related to life history stage; LW insects
may not eat much food during migration, but require more
food once reproduction begins. Flight capable insects are
presumptive dispersers, and they may fly over a long dis-
tance to find a suitable new habitat. Due to spatial hetero-
geneity, there might be a large area where food may not be
sufficient between one habitat and another. This physiolog-
ical trait would allow them to solve the problem and reach a
suitable new habitat successfully. After settling down, they
will need to consume more food in order to provide enough
nutrients for rapid reproduction.
Trade-off between flight capability and reproduction has
been considered one of the strongest evidence supporting
life history theory that when different traits are energeti-
cally costly, some traits may be emphasized at the expense
of others (Roff 1986; Zera and Denno 1997; Zera and
Harshman 2001). Our findings suggest that flight time may
serve as a signal for LW V. aspersus to switch from dis-
persal to reproduction, and trade-off between flight ability
and reproduction may be attenuated when flight time
reaches a critical threshold. Because average pre-oviposi-
tion period of SW female was 12.8 days (Zeng et al. 2012),
enhanced reproduction caused by flight in early adulthood
may potentially negates time advantage that SW animals
would have for reproduction relative to LW animals. In
most insect species, flight ability could be influenced by
age (Blackmer and Byrne 1993); therefore a flight of same
length may have a different effect on reproduction in ani-
mals with different age. However, in most wing polymor-
phic insect species, trade-off between flight and
reproduction are obvious only in early adulthood, and LW
animals would suffer a cost in reproduction whether or not
flight could promote reproduction in aged animals. For this
reason, only LW animals aged 3 days after emergence
were tested. Further study is needed to find out whether this
critical flight time is influenced by age or other factors.
Acknowledgments This work is supported by the National Nature
Science Foundation of China (Grant No. 31070586). The authors
thank Dr. Zhi-Wei Liu of Eastern Illinois University (USA) for
revising manuscript.
References
Andersen, N. M. (1982). The semi-aquatic bugs (Hemiptera. Gerri-
morpha) phylogeny, adaptations, biogeography and classifica-
tion. In Entomonograph (p 455), vol. 3, Klampenborg:
Scandinavian Science Press.
Arnett, R. H. (1985). American insects. New York: Van Nostrand
Reinhold Company.
Bertram, S. M. (2007). Positive relationship between signaling time
and flight capability in the Texas field cricket, Gryllus texensis.
Ethology, 113, 875–880.
Blackmer, J. L., & Byrne, D. N. (1993). Flight behaviour of Bemisia
tabaci in a vertical flight chamber: Effect of time of day, sex, age
and host quality. Physiological Entomology, 18, 223–232.
Colless, D. H., & McAlpine, D. K. (1970). Diptera (flies). In Insects
of Australia (CSIR0), (pp. 656–740), Melbourne: Melbourne
University Press.
Crnokrak, P., & Roff, D. A. (2000). The trade-off to macroptery in the
cricket Gryllus firmus: A path analysis in males. Journal of
Evolutionary Biology, 13, 396–408.
Dingle, H., & Arora, G. (1973). Experimental studies of migration in
bugs of the genus Dysdercus.Oecologia, 12, 119–140.
Dyakonova, V., & Krushinsky, A. (2008). Previous motor experience
enhances courtship behavior in male cricket Gryllus bimacula-
tus.Journal of Insect Behavior, 21, 172–180.
Guerra, P. A. (2011). Evaluating the life-history trade-off between
dispersal capability and reproduction in wing dimorphic insects:
A meta-analysis. Biological Reviews, 86, 813–835.
Guerra, P. A., & Pollack, G. S. (2007). A life history trade-off
between flight ability and reproductive behavior in male field
crickets (Gryllus texensis). Journal of Insect Behavior, 20,
377–387.
Guerra, P. A., & Pollack, G. S. (2009). Flight behaviour attenuates the
trade-off between flight capability and reproduction in a wing
polymorphic cricket. Biology Letters, 5, 229–231.
Gurney, A. B. (1938). A synopsis of the order Zoraptera with notes on
the biology of Zorotypus Hubbardi Caudell. Proceedings of the
Entomological Society of Washington, 40, 57–87.
402 Evol Biol (2014) 41:397–403
123
Author's personal copy
Harrison, R. G. (1980). Dispersal polymorphisms in insects. Annual
Review of Ecology Evolution and Systematics, 11, 95–118.
Jiang, X. F., Luo, L. Z., & Sappington, T. W. (2010). Relationship of
flight and reproduction in beet armyworm, Spodoptera exigua
(Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight
syndrome. Journal of Insect Physiology, 56, 1631–1637.
Mackerras, M. J. (1970). Blattodea (cockroaches). In Insects of
Australia (CSIR0), (pp. 262–274), Melbourne: Melbourne Uni-
versity Press.
McAnelly, M. L., & Rankin, M. A. (1986). Migration in the
grasshopper Melanoplus sanguinipes (Fab.) II. Interactions
between flight and reproduction. The Biological Bulletin, 170,
378–392.
Mole, S., & Zera, A. J. (1993). Deferential allocation of resources
underlies the dispersal-reproduction trade-off in the wing-
dimorphic cricket, Gryllus rubens.Oecologia, 93, 121–127.
Mole, S., & Zera, A. J. (1994). Differential resource consumption
obviates a potential flight–fecundity trade-off in the sand cricket
(Gryllus firmus). Functional Ecology, 8, 573–580.
Penner, M. (1985). Hormonal effects on flight and migration. In G.
A. Kerkut & L. I. Gilbert (Eds.), Comprehensive insect
physiology, biochemistry and pharmacology (pp. 491–550).
New York: Pergamon Press.
Roff, D. A. (1977). Dispersal in dipterans: Its costs and consequences.
Journal of Animal Ecology, 46, 443–456.
Roff, D. A. (1984). The cost of being able to fly: A study of wing
polymorphism in two species of crickets. Oecologia, 63, 30–37.
Roff, D. A. (1986). The evolution of wing dimorphism in insects.
Evolution, 40, 1009–1020.
Roff, D. A. (1989). Exaptation and the evolution of dealation in
insects. Journal of Evolutionay Biology, 2, 109–123.
Tanaka, S. (1976). Wing polymorphism, egg production and adult
longevity in Pteronemobius taprobanensis Walker (Orthoptera:
Gryllidae). Kontyuˆ, 44, 327–333.
Tanaka, S. (1991). Dealation and its influences on egg production and
flight muscle histolysis in a cricket (Velarifictorus parvus) that
undergoes inter-reproductive migration. Journal of Insect Phys-
iology, 37, 517–523.
Tanaka, S. (1993). Allocation of resources to egg production and
flight muscle development in a wing dimorphic cricket, Mod-
icogryllus confirmatus.Journal of Insect Physiology, 39,
493–498.
Walters, K. F. A., & Dixon, A. F. G. (1983). Migratory urge and
reproductive investment in aphids: Variation within clones.
Oecologia, 58, 70–75.
Zeng, Y., Zhu, D. H., & Zhao, L. Q. (2012). Trade-off between flight
capability and reproduction in male Velarifictorus aspersus
crickets. Ecological Entomology, 37, 244–251.
Zera, A. J. (1984). Difference in survivorship, development rate and
fecundity between the long winged and wingless morphs of the
water strider, Limnoporus canaliculatus.Evolution, 38,
1023–1032.
Zera, A. J., & Denno, R. F. (1997). Physiology and ecology of
dispersal polymorphism in insects. Annual Review of Entomol-
ogy, 42, 207–231.
Zera, A. J., & Harshman, L. G. (2001). The physiology of life history
trade-offs in animals. Annual Review of Ecology Evolution and
Systematics, 32, 95–126.
Zera, A. J., & Rankin, M. A. (1989). Wing dimorphism in Gryllus
rubens: Genetic basis of morph determination and fertility
differences between morphs. Oecologia, 80, 249–255.
Zera, A. J., Zhao, Z., & Kaliseck, K. (2007). Hormones in the field:
Evolutionary endocrinology of juvenile hormone and ecdyster-
oids in field populations of the wingdimorphic cricket Gryllus
firmus.Physiological and Biochemical Zoology, 80, 592–606.
Evol Biol (2014) 41:397–403 403
123
Author's personal copy
