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      Life Stage‐ and Sex‐Specific Sensitivity to Nutritional Stress in a Holometabolous Insect

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          ABSTRACT

          Over lifetime, organisms can be repeatedly exposed to stress, shaping their phenotype. At certain, so‐called sensitive phases, individuals might be more receptive to such stress, for example, nutritional stress. However, little is known about how plastic responses differ between individuals experiencing nutritional stress early versus later in life or repeatedly, particularly in species with distinct ontogenetic niches. Moreover, there may be sex‐specific differences due to distinct physiology. Larvae of the holometabolous turnip sawfly, Athalia rosae, consume leaves and flowers, while the adults take up nectar. We examined the effects of starvation experienced at different life stages on life‐history, adult behavioural and metabolic traits to determine which stage may be more sensitive and how specific these traits respond. We exposed individuals to four nutritional regimes, either no, larval, adult starvation or starvation periods as larvae and adults. Larvae exposed to starvation had a prolonged development, and starved females reached a lower initial adult body mass than non‐starved individuals. Males did not differ in initial adult body mass regardless of larval starvation, suggesting the ability to conform well to poor nutritional conditions. Adult behavioural activity was not significantly impacted by larval or adult starvation. Individuals starved as larvae had similar carbohydrate and lipid (i.e., fatty acid) contents as non‐starved individuals, potentially due to building up energy reserves during development, while starvation during adulthood or at both stages led to reduced energy reserves in males. This study indicates that the sensitivity of a life stage to stress depends on the specific trait under consideration. Life‐history traits were mainly affected by larval stress, while activity appeared to be more robust and metabolism mostly impacted by the adult conditions. Individuals differed in their ability to conform to the given environment, with the responses being life stage‐ and sex‐specific.

          Abstract

          Our study provides novel insights into trait‐specific sensitivity to nutritional stress across sex and life stages. By integrating life‐history, behaviour and metabolism, we explore mechanisms on an individual level, offering a comprehensive view of how these traits influence ecological patterns across ontogenetic niches of a holometabolous insect.

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          Most cited references65

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          Early growth conditions, phenotypic development and environmental change.

          Phenotypic development is the result of a complex interplay involving the organism's own genetic make-up and the environment it experiences during development. The latter encompasses not just the current environment, but also indirect, and sometimes lagged, components that result from environmental effects on its parents that are transmitted to their developing offspring in various ways and at various stages. These environmental effects can simply constrain development, for example, where poor maternal condition gives rise to poorly provisioned, low-quality offspring. However, it is also possible that environmental circumstances during development shape the offspring phenotype in such a way as to better prepare it for the environmental conditions it is most likely to encounter during its life. Studying the extent to which direct and indirect developmental responses to environmental effects are adaptive requires clear elucidation of hypotheses and careful experimental manipulations. In this paper, I outline how the different paradigms applied in this field relate to each other, the main predictions that they produce and the kinds of experimental data needed to distinguish among competing hypotheses. I focus on birds in particular, but the theories discussed are not taxon specific. Environmental influences on phenotypic development are likely to be mediated, in part at least, by endocrine systems. I examine evidence from mechanistic and functional avian studies and highlight the general areas where we lack key information.
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            Sex-specific fitness effects of nutrient intake on reproduction and lifespan.

            Diet affects both lifespan and reproduction [1-9], leading to the prediction that the contrasting reproductive strategies of the sexes should result in sex-specific effects of nutrition on fitness and longevity [6, 10] and favor different patterns of nutrient intake in males and females. However, males and females share most of their genome and intralocus sexual conflict may prevent sex-specific diet optimization. We show that both male and female longevity were maximized on a high-carbohydrate low-protein diet in field crickets Teleogryllus commodus, but male and female lifetime reproductive performances were maximized in markedly different parts of the nutrient intake landscape. Given a choice, crickets exhibited sex-specific dietary preference in the direction that increases reproductive performance, but this sexual dimorphism in preference was incomplete, with both sexes displaced from the optimum diet for lifetime reproduction. Sexes are, therefore, constrained in their ability to reach their sex-specific dietary optima by the shared biology of diet choice. Our data suggest that sex-specific selection has thus far failed fully to resolve intralocus sexual conflict over diet optimization. Such conflict may be an important factor linking nutrition and reproduction to lifespan and aging.
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              Compensation for a bad start: grow now, pay later?

              Nutritional conditions during key periods of development, when the architecture and modus operandi of the body become established, are of profound importance in determining the subsequent life-history trajectory of an organism. If developing individuals experience a period of nutritional deficit, they can subsequently show accelerated growth should conditions improve, apparently compensating for the initial setback. However, recent research suggests that, although compensatory growth can bring quick benefits, it is also associated with a surprising variety of costs that are often not evident until much later in adult life. Clearly, the nature of these costs, the timescale over which they are incurred and the mechanisms underlying them will play a crucial role in determining compensatory strategies. Nonetheless, such effects remain poorly understood and largely neglected by ecologists and evolutionary biologists.
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                Author and article information

                Contributors
                caroline.mueller@uni-bielefeld.de
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                18 January 2025
                January 2025
                : 15
                : 1 ( doiID: 10.1002/ece3.v15.1 )
                : e70764
                Affiliations
                [ 1 ] Department of Chemical Ecology Bielefeld University Bielefeld Germany
                [ 2 ] Joint Institute for Individualisation in a Changing Environment (JICE) University of Münster and Bielefeld University Bielefeld Germany
                Author notes
                [*] [* ] Correspondence:

                Caroline Müller ( caroline.mueller@ 123456uni-bielefeld.de )

                Author information
                https://orcid.org/0000-0002-1276-4345
                https://orcid.org/0000-0002-7411-3206
                https://orcid.org/0000-0002-8447-534X
                Article
                ECE370764 ECE-2024-09-01992.R1
                10.1002/ece3.70764
                11748456
                39839333
                36c61b8b-348a-4b1c-8c5e-47bd8b02e9ff
                © 2025 The Author(s). Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 November 2024
                : 23 September 2024
                : 12 December 2024
                Page count
                Figures: 7, Tables: 0, Pages: 10, Words: 7000
                Funding
                Funded by: Deutsche Forschungsgemeinschaft , doi 10.13039/501100001659;
                Award ID: 396777467
                Categories
                Behavioural Ecology
                Research Article
                Research Article
                Custom metadata
                2.0
                January 2025
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.5.2 mode:remove_FC converted:18.01.2025

                Evolutionary Biology
                behaviour,energy metabolism,life‐history,niche conformance,phenotypic plasticity,sensitive phases,starvation

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