Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly<i>Rhagoletis pomonella</i>

Ragland, Gregory J.; Egan, Scott P.; Feder, Jeffrey L.; Berlocher, Stewart H.; Hahn, Daniel A.

doi:10.1242/jeb.061085

Cited by 133 publications

(135 citation statements)

References 85 publications

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“…Similar results were found in flies (Emerson et al, 2010;Poelchau et al, 2011;Ragland et al, 2010Ragland et al, , 2011. This suggests a conserved transcriptional basis for the end of the diapause developmental pathway, despite ∼200 million years of divergence (Pringle et al, 2007) and distinct diapausing life-stages (larval versus pupal) in different environments (host plant versus soil).…”

Section: Global Transcriptional Patternssupporting

confidence: 77%

“…Previous results in flies suggest that a common characteristic of diapause is cell-cycle arrest in the G0/G1 or G2 phases, with transition into cell cycle progression being indicative of the end of diapause (Koštál et al, 2009;Ragland et al, 2010Ragland et al, , 2011. Gene expression profiles in corn borers support a transition into active cell cycling upon exposure to long-day cues in the E-strain but not the (Fig.…”

Section: Release From Developmental Arrestmentioning

confidence: 72%

“…Cell cycling, DNA replication/transcription and stress response genes have been proposed to be important for diapause initiation in moths and mosquitos (Bao and Xu, 2011;Poelchau et al, 2011). Additionally, genes in the Wnt and TOR signaling pathways have been nominated as strong regulatory candidates during diapause termination in Rhagoletis flies (Ragland et al, 2011). Perhaps the best single candidate thus far identified is for the egg diapause of the silkmoth (Bombyx mori), in which transgenerational diapause induction involves the temperature-sensitive Transient receptor potential A1 (Trpa1) gene (Sato et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

Wadsworth

Dopman

2015

Journal of Experimental Biology

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Rapid evolutionary change in seasonal timing can facilitate ecological speciation and resilience to climate warming. However, the molecular mechanisms behind shifts in animal seasonality are still unclear. Evolved differences in seasonality occur in the European corn borer moth (Ostrinia nubilalis), in which early summer emergence in E-strain adults and later summer emergence in Z-strain adults is explained by a shift in the length of the termination phase of larval diapause. Here, we sample from the developmental time course of diapause in both strains and use transcriptome sequencing to profile regulatory and amino acid changes associated with timing divergence. Within a previously defined quantitative trait locus (QTL), we nominate 48 candidate genes, including several in the insulin signaling and circadian rhythm pathways. Genome-wide transcriptional activity is negligible during the extended Z-strain termination, whereas shorter E-strain termination is characterized by a rapid burst of regulatory changes involved in resumption of the cell cycle, hormone production and stress response. Although gene expression during diapause termination in Ostrinia is similar to that found previously in flies, nominated genes for shifts in timing are species specific. Hence, across distant relatives the evolution of insect seasonality appears to involve unique genetic switches that direct organisms into distinct phases of the diapause pathway through wholesale restructuring of conserved gene regulatory networks.

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Section: Global Transcriptional Patternssupporting

confidence: 77%

Section: Release From Developmental Arrestmentioning

confidence: 72%

Section: Introductionmentioning

confidence: 99%

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Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

Wadsworth

Dopman

2015

Journal of Experimental Biology

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“…3A,B). This indicates that diapause reflects a temporal removal from the direct development trajectory, as also seen in, for instance, Rhagoletis pomonella (Ragland et al, 2009(Ragland et al, , 2011. Directly developing pupae and diapausing pupae showed similarly decreasing MR trajectories after the first days of pupation, which probably reflects apoptotic breakdown of larval tissues (Schmolz and Lamprecht, 2000).…”

Section: Mrmentioning

confidence: 70%

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

Lehmann

Pruisscher

Posledovich

et al. 2016

Journal of Experimental Biology

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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.

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“…2013) and the apple maggot fly (Ragland et al. 2011). We used a stop‐flow system to measure CO 2 production over the course of a night, recording the amount of CO 2 expelled over the duration of one cycle, which was 45 min for individuals from the 30 to 120 days treatment, and 25 min for individuals from the 150 days treatment.…”

Section: Discussionmentioning

confidence: 99%

Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines

Stålhandske

Lehmann

Pruisscher

et al. 2015

Ecology and Evolution

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The effect of spring temperature on spring phenology is well understood in a wide range of taxa. However, studies on how winter conditions may affect spring phenology are underrepresented. Previous work on Anthocharis cardamines (orange tip butterfly) has shown population‐specific reaction norms of spring development in relation to spring temperature and a speeding up of post‐winter development with longer winter durations. In this experiment, we examined the effects of a greater and ecologically relevant range of winter durations on post‐winter pupal development of A. cardamines of two populations from the United Kingdom and two from Sweden. By analyzing pupal weight loss and metabolic rate, we were able to separate the overall post‐winter pupal development into diapause duration and post‐diapause development. We found differences in the duration of cold needed to break diapause among populations, with the southern UK population requiring a shorter duration than the other populations. We also found that the overall post‐winter pupal development time, following removal from winter cold, was negatively related to cold duration, through a combined effect of cold duration on diapause duration and on post‐diapause development time. Longer cold durations also lead to higher population synchrony in hatching. For current winter durations in the field, the A. cardamines population of southern UK could have a reduced development rate and lower synchrony in emergence because of short winters. With future climate change, this might become an issue also for other populations. Differences in winter conditions in the field among these four populations are large enough to have driven local adaptation of characteristics controlling spring phenology in response to winter duration. The observed phenology of these populations depends on a combination of winter and spring temperatures; thus, both must be taken into account for accurate predictions of phenology.

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Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot flyRhagoletis pomonella

Cited by 133 publications

References 85 publications

Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

Transcriptome profiling reveals mechanisms for the evolution of insect seasonality

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

Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines

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