RESEARCH ARTICLE
Heat- and humidity-induced plastic changes in body lipids and
starvation resistance in the tropical fly Zaprionus indianus during
wet and dry seasons
T. N. Girish
1
, B. E. Pradeep
1
and Ravi Parkash
2,
*
ABSTRACT
Insects in tropical wet or dry seasons are likely to cope with starvation
stress through plastic changes (developmental as well as adult
acclimation) in energy metabolites. Control and experimental groups
of Zaprionus indianus flies were reared under wet or dry conditions,
but adults were acclimated at different thermal or humidity conditions.
Adult flies of the control group were acclimated at 27°C and low (50%)
or high (60%) relative humidity (RH). For experimental groups, adult
flies were acclimated at 32°C for 1 to 6 days and under low (40%) or
high (70%) RH. For humidity acclimation, adult flies were acclimated
at 27°C but under low (40%) or high (70%) RH for 1 to 6 days. Plastic
changes in experimental groups as compared with the control group
(developmental as well as adult acclimation) revealed significant
accumulation of body lipids owing to thermal or humidity acclimation
of wet season flies, but low humidity acclimation did not change the
level of body lipids in dry season flies. Starvation resistance and body
lipids were higher in the males of dry season flies but in the females
of wet season flies. Adults acclimated under different thermal or
humidity conditions exhibited changes in the rate of utilization of body
lipids, carbohydrates and proteins. Adult acclimation of wet or dry
season flies revealed plastic changes in mean daily fecundity; and a
reduction in fecundity under starvation. Thus, thermal or humidity
acclimation of adults revealed plastic changes in energy metabolites
to support starvation resistance of wet or dry season flies.
KEY WORDS: Tropical drosophilid, Developmental acclimation,
Adult acclimation, Heat acclimation, Humidity acclimation
INTRODUCTION
In the wild habitats of diverse insect taxa, incidence of food shortage
is associated with seasonal changes in abiotic conditions (Tauber
et al., 1986; Danks, 2004). Several studies have shown heritable
variation in starvation resistance in diverse insect taxa (see Rion and
Kawecki, 2007). Genetic variation for starvation resistance has been
examined in different Drosophila species (Matzkin et al., 2009a), in
geographical populations of D. melanogaster (Hoffmann and
Parsons, 1991; Parkash and Munjal, 1999; Robinson et al., 2000;
Hoffmann et al., 2001) and on the basis of laboratory selection
experiments (Chippindale et al., 1996; Hoffmann et al., 2005). In
contrast, stress-induced plastic changes in starvation resistance have
been investigated mainly in D. melanogaster (1) on the basis of adult
flies acclimated to different stressors (Bubliy et al., 2012) and
regarding (2) the developmental acclimation effects of constant
versus summer-simulated conditions (Hoffmann et al., 2005), (3) the
developmental acclimation effects of different humidity levels
(Parkash et al., 2014b) and (4) the lack of geographical differences
in plastic responses for starvation resistance of D. leontia (Aggarwal,
2014). Developmental acclimation under summer-specific thermal
conditions revealed higher starvation resistance compared with
acclimation under winter conditions (Hoffmann et al., 2005).
Further, D. melanogaster flies reared in high humidity evidenced
an increase in resistance to heat as well as to starvation (Parkash et al.,
2014b). Adult acclimation of D. melanogaster flies reared under
standard growth conditions showed a lack of cross-tolerance between
starvation and resistance to heat or cold (Bubliy et al., 2012).
However, these previous studies did not consider combined
acclimation effects resulting from developmental as well as adult
acclimation. Such combined plastic effects for starvation resistance
are likely to reflect acclimatization of flies in wild habitats.
In ectothermic organisms, seasonally varying thermal conditions
induce plastic responses for morphological and life history traits
(Bochdanovits and de Jong, 2003; de Jong, 2005, 2010; Behrman
et al., 2015). Both thermal and humidity conditions vary
significantly in subtropical regions. In the tropics, wet or dry
seasons differ approximately two-fold in relative humidity, but
thermal changes are limited. Seasonal phenotypic plasticity in
tropical climates has been demonstrated for wing pattern
polyphenism in the African butterfly Bicyclus anynana (Roskam
and Brakefield, 1999) and for drought resistance in the mosquito
Anopheles gambiae from Africa (Wagoner et al., 2014) and in
Drosophila leontia (Parkash and Ranga, 2014). In tropical insect
taxa, wet or dry conditions are likely to elicit seasonal phenotypic
plasticity of starvation resistance, which has received little attention
in the literature thus far. However, a single study has investigated
seasonal phenotypic plasticity of starvation resistance in a sub-
tropical African butterfly, Bicyclus anynana (Pijpe et al., 2007). In
B. anynana, there are wet or dry seasonal morphs that vary in body
coloration as well as in reproductive behaviour, i.e. they have two
extended generations per year, and show higher fecundity in the wet
season morph than in the dry season morph. Bicyclus anynana from
that study showed greater starvation resistance in the dry season
morph (living under the cooler, autumn and winter temperature of
18°C) than in the wet season morph (spring and summer
temperature of 27°C). Seasonal plastic differences in starvation
resistance of B. anynana revealed associated changes in resting
metabolic rate: adult butterflies acclimated at 27°C had higher
resting metabolic rates (CO
2
production) than butterflies acclimated
at 18°C. However, Pijpe et al. (2007) did not investigate the plastic
effects of humidity acclimation or plastic changes in the energy
Received 16 November 2017; Accepted 20 March 2018
1
Department of Biosciences, Sri Sathya Sai Institute of Higher Learning, Prasanthi
Nilayam 515134, India.
2
Department of Genetics, Maharshi Dayanand University,
Rohtak 124001, India.
*Author for correspondence (rpgenetics@gmail.com)
T.N.G., 0000-0002-5048-5283; B.E.P., 0000-0001-8022-8168; R.P., 0000-0001-
9880-3941
1
© 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb174482. doi:10.1242/jeb.174482
Journal of Experimental Biology