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Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions

Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions
Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions

Although environmental variability and predictability have been proposed as the underlying ecological context in which transgenerational plasticity (TGP) arises, the adaptive significance and interaction with within-generation plasticity (WGP) in such scenarios is still poorly understood. To investigate these questions, we considered the tolerance to upper thermal limits of larvae and adults of the desert endemic Drosophila mojavensis adapted to different climatic regions (Desert vs. Mediterranean climate). Thermal plasticity was investigated by acclimating parents and offspring at 36°C (vs. at 25°C). We then used historical temperature variation data from both regions to perform individual-based simulations by modelling expected components of adaptive plasticity in multiple life stages. Our results indicated that thermal response to ramping heat shocks was more pronounced in larvae, where acclimation treatments in parents and offspring increased their heat-shock performance, while heat knockdown in adults was only increased by offspring acclimation of adults. The relative contribution of WGP and TGP was greater for the population from the more thermally variable Sonoran Desert. Similarly, individual-based simulations of evolving maternal effects indicated that variation in tolerance to upper thermal limits across life stages and climates is expected from its adaptive significance in response to environmental predictability. Our approach offers a new perspective and interpretation of adaptive plasticity, demonstrating that environmental predictability can drive thermal responses across generations and life stages in a scenario with regional climate variability. A free Plain Language Summary can be found within the Supporting Information of this article.

Drosophila mojavensis, acclimation, carry-over effects, heat-shock tolerance, individual-based simulations, within/transgenerational plasticity
0269-8463
153-166
Diaz, Fernando
f44303b6-95df-4525-9a3d-2d75a0e3b7a2
Kuijper, Bram
f19c6018-c796-4a9a-97f3-30e3d8abe7dd
Hoyle, Rebecca
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Talamantes, Nathaniel
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Coleman, Joshua
71534299-e7e4-40d2-b80b-8e33ada45804
Matzkin, Luciano
5f29e79f-3353-4fb8-879d-759a5c340992
Diaz, Fernando
f44303b6-95df-4525-9a3d-2d75a0e3b7a2
Kuijper, Bram
f19c6018-c796-4a9a-97f3-30e3d8abe7dd
Hoyle, Rebecca
e980d6a8-b750-491b-be13-84d695f8b8a1
Talamantes, Nathaniel
5a8c5eb9-2d24-4ae8-8a6d-20096bdedded
Coleman, Joshua
71534299-e7e4-40d2-b80b-8e33ada45804
Matzkin, Luciano
5f29e79f-3353-4fb8-879d-759a5c340992

Diaz, Fernando, Kuijper, Bram, Hoyle, Rebecca, Talamantes, Nathaniel, Coleman, Joshua and Matzkin, Luciano (2021) Environmental predictability drives adaptive within‐ and transgenerational plasticity of heat tolerance across life stages and climatic regions. Functional Ecology, 35 (1), 153-166. (doi:10.1111/1365-2435.13704).

Record type: Article

Abstract

Although environmental variability and predictability have been proposed as the underlying ecological context in which transgenerational plasticity (TGP) arises, the adaptive significance and interaction with within-generation plasticity (WGP) in such scenarios is still poorly understood. To investigate these questions, we considered the tolerance to upper thermal limits of larvae and adults of the desert endemic Drosophila mojavensis adapted to different climatic regions (Desert vs. Mediterranean climate). Thermal plasticity was investigated by acclimating parents and offspring at 36°C (vs. at 25°C). We then used historical temperature variation data from both regions to perform individual-based simulations by modelling expected components of adaptive plasticity in multiple life stages. Our results indicated that thermal response to ramping heat shocks was more pronounced in larvae, where acclimation treatments in parents and offspring increased their heat-shock performance, while heat knockdown in adults was only increased by offspring acclimation of adults. The relative contribution of WGP and TGP was greater for the population from the more thermally variable Sonoran Desert. Similarly, individual-based simulations of evolving maternal effects indicated that variation in tolerance to upper thermal limits across life stages and climates is expected from its adaptive significance in response to environmental predictability. Our approach offers a new perspective and interpretation of adaptive plasticity, demonstrating that environmental predictability can drive thermal responses across generations and life stages in a scenario with regional climate variability. A free Plain Language Summary can be found within the Supporting Information of this article.

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Diaz_et_al_accepted_manuscript - Accepted Manuscript
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More information

Accepted/In Press date: 28 September 2020
e-pub ahead of print date: 16 October 2020
Published date: 8 January 2021
Keywords: Drosophila mojavensis, acclimation, carry-over effects, heat-shock tolerance, individual-based simulations, within/transgenerational plasticity

Identifiers

Local EPrints ID: 444835
URI: http://eprints.soton.ac.uk/id/eprint/444835
ISSN: 0269-8463
PURE UUID: 6e06d810-b9ca-499c-9e89-6713927b8c11
ORCID for Rebecca Hoyle: ORCID iD orcid.org/0000-0002-1645-1071

Catalogue record

Date deposited: 06 Nov 2020 17:30
Last modified: 26 Nov 2021 06:57

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Contributors

Author: Fernando Diaz
Author: Bram Kuijper
Author: Rebecca Hoyle ORCID iD
Author: Nathaniel Talamantes
Author: Joshua Coleman
Author: Luciano Matzkin

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