Sex-specific divergence for adaptations to dehydration stress in Drosophila kikkawai

Abstract

SUMMARYSeveral studies on diverse Drosophila species have reported higher desiccation resistance of females, but the physiological basis of such sex-specific differences has received less attention. We tested whether sex-specific differences in cuticular traits (melanic females and non-melanic males) of Drosophila kikkawai correspond with divergence in their water balance mechanisms. Our results are interesting in several respects. First, positive clinal variation in desiccation resistance was correlated with cuticular melanisation in females but with changes in cuticular lipid mass in males, despite a lack of differences between the sexes for the rate of water loss. Second, a comparative analysis of water budget showed that females of the northern population stored more body water as well as hemolymph content and exhibited greater dehydration tolerance than flies from the southern tropics. In contrast, we found no geographical variation in the males for water content and dehydration tolerance. Third, an ~10-fold increase in the rate of water loss after organic solvent treatment of male D. kikkawai suggested a role of cuticular lipids in cuticular transpiration, but had no effect in the females. Fourth, geographical differences in the storage of carbohydrate content (metabolic fuel) were observed in females but not in males. Interestingly, in females, the rate of utilization of carbohydrates did not vary geographically, but males from drier localities showed a 50% reduction compared with wetter localities. Thus, body melanisation, increased body water, hemolymph, carbohydrate content and greater dehydration tolerance confer greater desiccation resistance in females, but a reduced rate of water loss is the only possible mechanism to cope with drought stress in males. Finally, acclimated females showed a significant increase in drought resistance associated with higher trehalose content as well as dehydration tolerance, while males showed no acclimation response. Thus, sex-specific differences in desiccation resistance of D. kikkawai are associated with divergence in some water balance strategies, despite a lack of differences in the rate of water loss between the two sexes.

Adaptive patterns of phenotypic plasticity in laboratory and field environments in Drosophila melanogaster

“…The observed effects of physiological acclimation to both high-and low-temperature conditions on stress tolerance are consistent with temperature being a major factor in modulating subsequent performance and fitness in D. melanogaster (e.g., Cossins et al 2002;Kristensen et al 2003;Hoffmann et al 2005a Parkash and Ranga 2013). Similarly, exposure to distinct, seasonal photoperiods had predictable effects on multiple aspects of stress tolerance.…”

“…; Kristensen et al. ; Sisodia and Singh ; Parkash and Ranga ). Similarly, exposure to distinct, seasonal photoperiods had predictable effects on multiple aspects of stress tolerance.…”

Desiccation tolerance as a function of age, sex, humidity and temperature in adults of the African malaria vectorsAnopheles arabiensisPatton andAnopheles funestusGiles

“…Such a response has not been documented across a wide variety of insect groups, except for several species of Drosophila, and even here variation is typically among early and late life and also among species and sex (e.g. Matzkin et al, 2007;Shahrestani et al, 2012;Parkash and Ranga, 2013;Aggarwal, 2014). Mechanisms that might underlie a decline in tolerance with age are thought to include changes in WLR, probably a function of variation in cuticular hydrocarbon content and composition, melanization, differences in initial body water content and tolerance of dehydration (Nghiem et al, 2000;Gibbs and Markow, 2001;Benoit and Denlinger, 2007;Weldon et al, 2013).…”

“…First, cuticular WLR, which generally dominates loss (Chown et al, 2011), differs among the sexes, as confirmed by pronounced effect size differences between males and females for the influence of WLR on survival. In turn, these differences are likely to be a consequence of variation in cuticle lipid content and/or composition, or cuticle thickness (Parkash and Ranga, 2013;Parkash and Ranga, 2014). Although some evidence exists for thicker cuticles in female mosquitoes (Wood et al, 2010), it seems likely that variation in cuticular lipid amount and composition is more likely to account for variation in WLR (Reidenbach et al, 2014).…”

Cuticular differences associated with aridity acclimation in African malaria vectors carrying alternative arrangements of inversion 2La

“…While 2La inverted homokaryotypes boosted their mass-specific glycogen content and reduced lipid stores, the converse was true for 2L+ a homokaryotypes [17]. It is noteworthy that increased storage of glycogen, utilized by Drosophila under desiccation stress [29], has been associated with higher dehydration tolerance in flies [29-31], consistent with its proposed role as an osmolyte for water retention [30]. Taken together, these data suggest that genes inside the 2La inversion influence water balance and desiccation resistance, but also that resistance to desiccation is a complex trait, whose precise physiological basis and causal genes remain to be elucidated.…”