Structural plasticity of olfactory neuropils in relation to insect diapause

Abstract Many insects that live in temperate zones spend the cold season in a state of dormancy, referred to as diapause. As the insect must rely on resources that were gathered before entering diapause, keeping a low metabolic rate is of utmost importance. Organs that are metabolically expensive to...

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Main Authors: Maertha Eriksson, Niklas Janz, Sören Nylin, Mikael A. Carlsson
Format: Article
Language:English
Published: Wiley 2020-12-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.7046
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spelling doaj-def586381be54d5682f883539b9fa03b2021-06-04T07:10:38ZengWileyEcology and Evolution2045-77582020-12-011024144231443410.1002/ece3.7046Structural plasticity of olfactory neuropils in relation to insect diapauseMaertha Eriksson0Niklas Janz1Sören Nylin2Mikael A. Carlsson3Department of Zoology Stockholm University Stockholm SwedenDepartment of Zoology Stockholm University Stockholm SwedenDepartment of Zoology Stockholm University Stockholm SwedenDepartment of Zoology Stockholm University Stockholm SwedenAbstract Many insects that live in temperate zones spend the cold season in a state of dormancy, referred to as diapause. As the insect must rely on resources that were gathered before entering diapause, keeping a low metabolic rate is of utmost importance. Organs that are metabolically expensive to maintain, such as the brain, can therefore become a liability to survival if they are too large. Insects that go through diapause as adults generally do so before entering the season of reproduction. This order of events introduces a conflict between maintaining low metabolism during dormancy and emerging afterward with highly developed sensory systems that improve fitness during the mating season. We investigated the timing of when investments into the olfactory system are made by measuring the volumes of primary and secondary olfactory neuropils in the brain as they fluctuate in size throughout the extended diapause life‐period of adult Polygonia c‐album butterflies. Relative volumes of both olfactory neuropils increase significantly during early adult development, indicating the importance of olfaction to this species, but still remain considerably smaller than those of nondiapausing conspecifics. However, despite butterflies being kept under the same conditions as before the dormancy, their olfactory neuropil volumes decreased significantly during the postdormancy period. The opposing directions of change in relative neuropil volumes before and after diapause dormancy indicate that the investment strategies governing structural plasticity during the two life stages could be functionally distinct. As butterflies were kept in stimulus‐poor conditions, we find it likely that investments into these brain regions rely on experience‐expectant processes before diapause and experience‐dependent processes after diapause conditions are broken. As the shift in investment strategies coincides with a hard shift from premating season to mating season, we argue that these developmental characteristics could be adaptations that mitigate the trade‐off between dormancy survival and reproductive fitness.https://doi.org/10.1002/ece3.7046antennal lobebrainbutterflydiapauseinsectmushroom body
collection DOAJ
language English
format Article
sources DOAJ
author Maertha Eriksson
Niklas Janz
Sören Nylin
Mikael A. Carlsson
spellingShingle Maertha Eriksson
Niklas Janz
Sören Nylin
Mikael A. Carlsson
Structural plasticity of olfactory neuropils in relation to insect diapause
Ecology and Evolution
antennal lobe
brain
butterfly
diapause
insect
mushroom body
author_facet Maertha Eriksson
Niklas Janz
Sören Nylin
Mikael A. Carlsson
author_sort Maertha Eriksson
title Structural plasticity of olfactory neuropils in relation to insect diapause
title_short Structural plasticity of olfactory neuropils in relation to insect diapause
title_full Structural plasticity of olfactory neuropils in relation to insect diapause
title_fullStr Structural plasticity of olfactory neuropils in relation to insect diapause
title_full_unstemmed Structural plasticity of olfactory neuropils in relation to insect diapause
title_sort structural plasticity of olfactory neuropils in relation to insect diapause
publisher Wiley
series Ecology and Evolution
issn 2045-7758
publishDate 2020-12-01
description Abstract Many insects that live in temperate zones spend the cold season in a state of dormancy, referred to as diapause. As the insect must rely on resources that were gathered before entering diapause, keeping a low metabolic rate is of utmost importance. Organs that are metabolically expensive to maintain, such as the brain, can therefore become a liability to survival if they are too large. Insects that go through diapause as adults generally do so before entering the season of reproduction. This order of events introduces a conflict between maintaining low metabolism during dormancy and emerging afterward with highly developed sensory systems that improve fitness during the mating season. We investigated the timing of when investments into the olfactory system are made by measuring the volumes of primary and secondary olfactory neuropils in the brain as they fluctuate in size throughout the extended diapause life‐period of adult Polygonia c‐album butterflies. Relative volumes of both olfactory neuropils increase significantly during early adult development, indicating the importance of olfaction to this species, but still remain considerably smaller than those of nondiapausing conspecifics. However, despite butterflies being kept under the same conditions as before the dormancy, their olfactory neuropil volumes decreased significantly during the postdormancy period. The opposing directions of change in relative neuropil volumes before and after diapause dormancy indicate that the investment strategies governing structural plasticity during the two life stages could be functionally distinct. As butterflies were kept in stimulus‐poor conditions, we find it likely that investments into these brain regions rely on experience‐expectant processes before diapause and experience‐dependent processes after diapause conditions are broken. As the shift in investment strategies coincides with a hard shift from premating season to mating season, we argue that these developmental characteristics could be adaptations that mitigate the trade‐off between dormancy survival and reproductive fitness.
topic antennal lobe
brain
butterfly
diapause
insect
mushroom body
url https://doi.org/10.1002/ece3.7046
work_keys_str_mv AT maerthaeriksson structuralplasticityofolfactoryneuropilsinrelationtoinsectdiapause
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AT sorennylin structuralplasticityofolfactoryneuropilsinrelationtoinsectdiapause
AT mikaelacarlsson structuralplasticityofolfactoryneuropilsinrelationtoinsectdiapause
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