Biphasic metabolic rate trajectory of pupal diapause termination and post-diapause development in a tephritid fly

Diapause is a fundamental component of the life cycle in the majority of insects living in environments characterized by strong seasonality. The present study addresses poorly understood associations and trade-offs between endogenous diapause duration, thermal sensitivity of development, energetic cost of development and cold tolerance. Diapause intensity, metabolic rate trajectories and lipid profiles of directly developing and diapausing animals were studied using pupae and adults of Pieris napi butterflies from a population in which endogenous diapause has been well studied. Endogenous diapause was terminated after 3 months and termination required chilling. Metabolic and post-diapause development rates increased with diapause duration, while the metabolic cost of post-diapause development decreased, indicating that once diapause is terminated, development proceeds at a low rate even at low temperature. Diapausing pupae had larger lipid stores than the directly developing pupae, and lipids constituted the primary energy source during diapause. However, during diapause, lipid stores did not decrease. Thus, despite lipid catabolism meeting the low energy costs of the diapausing pupae, primary lipid store utilization did not occur until the onset of growth and metamorphosis in spring. In line with this finding, diapausing pupae contained low amounts of mitochondria-derived cardiolipins, which suggests a low capacity for fatty acid β-oxidation. While ontogenic development had a large effect on lipid and fatty acid profiles, only small changes in these were seen during diapause. The data therefore indicate that the diapause lipidomic phenotype is developed early, when pupae are still at high temperature, and retained until post-diapause development.

Section: Mrmentioning

confidence: 67%

Energy and lipid metabolism during direct and diapause development in a pierid butterfly

Lehmann

Pruisscher

Posledovich

et al. 2016

“…Heads were pestlehomogenized and stored at −80°C for no more than 4 weeks before RNA was extracted using Ambion RiboPure kits following the manufacturer's recommendations. To confirm that pupae sampled after the shift to 23°C were still in diapause, we conducted stop-flow respirometry on each individual following Ragland et al (2009), using a LI-COR 6252 CO 2 analyzer (LI-COR Biosciences, Lincoln, NB, USA) coupled to Sable Systems pumping and metering components (Sable Systems International, Las Vegas, NV, USA) to measure metabolic rates prior to sampling at 24 and 48 h after the temperature shift. All pupae measured at 24 and 48 h exhibited metabolic rates indicative of diapause (supplement S1.1, deposited in Dryad; see 'Data availability', below).…”

Section: Experimental Designmentioning

confidence: 99%

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

Meyers

Powell

Walden

et al. 2016

Self Cite

The duration of dormancy regulates seasonal timing in many organisms and may be modulated by day length and temperature. Though photoperiodic modulation has been well studied, temperature modulation of dormancy has received less attention. Here, we leverage genetic variation in diapause in the apple maggot fly, Rhagoletis pomonella, to test whether gene expression during winter or following spring warming regulates diapause duration. We used RNAseq to compare transcript abundance during and after simulated winter between an apple-infesting population and a hawthorn-infesting population where the apple population ends pupal diapause earlier than the hawthorn-infesting population. Marked differences in transcription between the two populations during winter suggests that the 'early' apple population is developmentally advanced compared with the 'late' hawthorn population prior to spring warming, with transcripts participating in growth and developmental processes relatively up-regulated in apple pupae during the winter cold period. Thus, regulatory differences during winter ultimately drive phenological differences that manifest themselves in the following summer. Expression and polymorphism analysis identify candidate genes in the Wnt and insulin signaling pathways that contribute to population differences in seasonality. Both populations remained in diapause and displayed a pattern of up-and then down-regulation (or vice versa) of growth-related transcripts following warming, consistent with transcriptional repression. The ability to repress growth stimulated by permissive temperatures is likely critical to avoid mismatched phenology and excessive metabolic demand. Compared with diapause studies in other insects, our results suggest some overlap in candidate genes/pathways, though the timing and direction of changes in transcription are likely species specific.

“…It is believed, however, that similar physiological mechanisms are involved (Masaki, 1980;Denlinger, 1986;Benoit, 2010). Accordingly, the expected physiological changes that underlie aestivation include reduced reproduction, metabolic rate, feeding response and activity level, increased desiccation and temperature resistance, and increased nutritional reserves prior to the start of aestivation, as these characterize insect diapause (Masaki, 1980;Danks, 1987;Chown and Gaston, 1999;Blanckenhorn et al, 2001;Denlinger, 2002;Gray and Bradley, 2005;Huestis and Marshall, 2006;Kessler and Guerin, 2008;Ragland et al, 2009). Many insects also exhibit morphological variation in body size and/or coloration associated with diapause (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…This prediction is based only on winter diapause studies (e.g. Danks, 1987;Chown and Gaston, 1999;Guppy and Withers, 1999;Denlinger, 2002;Benoit and Denlinger, 2007;Ragland et al, 2009;Ragland et al, 2010) rather than on summer diapause, as no measurements of metabolic rate during insect aestivation are known to us. In contrast to summer aestivation, metabolism during winter diapause is reduced not only by the low ambient temperatures that insects experience but also by the insect's physiology (Danks, 1987;Layne and Eyck, 1996;Guppy and Withers, 1999;Denlinger, 2002;Canzano et al, 2006;Benoit and Denlinger, 2007;Ragland et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel

Huestis

Yaro

Traoré

et al. 2012

SUMMARYMalaria in Africa is vectored primarily by the Anopheles gambiae complex. Although the mechanisms of population persistence during the dry season are not yet known, targeting dry season mosquitoes could provide opportunities for vector control. In the Sahel, it appears likely that M-form A. gambiae survive by aestivation (entering a dormant state). To assess the role of ecophysiological changes associated with dry season survival, we measured body size, flight activity and metabolic rate of wildcaught mosquitoes throughout 1year in a Sahelian locality, far from permanent water sources, and at a riparian location adjacent to the Niger River. We found significant seasonal variation in body size at both the Sahelian and riparian sites, although the magnitude of the variation was greater in the Sahel. For flight activity, significant seasonality was only observed in the Sahel, with increased flight activity in the wet season when compared with that just prior to and throughout the dry season. Whole-organism metabolic rate was affected by numerous biotic and abiotic factors, and a significant seasonal component was found at both locations. However, assay temperature accounted completely for seasonality at the riparian location, while significant seasonal variation remained after accounting for all measured variables in the Sahel. Interestingly, we did not find that mean metabolic rate was lowest during the dry season at either location, contrary to our expectation that mosquitoes would conserve energy and increase longevity by reducing metabolism during this time. These results indicate that mosquitoes may use mechanisms besides reduced metabolic rate to enable survival during the Sahelian dry season. Supplementary material available online at