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Intergenerational Effects of Early Life Starvation on Life-History, Consumption, and Transcriptome of a Holometabolous Insect

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Intergenerational Effects of Early Life Starvation on Life-History, Consumption, and Transcriptome of a Holometabolous Insect bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434967; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Intergenerational Effects of Early Life Starvation on Life-History, Consumption, 2 and Transcriptome of a Holometabolous Insect 3 4 Sarah Catherine Paul1,a, Pragya Singh1,a, Alice B. Dennis2, Caroline Müller1* 5 6 1Chemical Ecology, Bielefeld University, Universitätsstr. 25, 33615 Bielefeld, 7 Germany 8 2 Evolutionary Biology & Systematic Zoology, University of Potsdam, Karl-Liebknecht- 9 Strasse 24-25, 14476 Potsdam 10 a shared first authorship 11 *corresponding author: [email protected] 12 13 Mail addresses: SCP: [email protected], PS: 14 [email protected], ABD: [email protected], CM: 15 [email protected] 16 The authors wish to be identified to the reviewers 17 18 Running title: Intergenerational effects on sawfly 19 20 Keywords 21 Intergenerational effects, sawfly, starvation, transcriptome, parental effects, 22 compensatory growth. 23 24 Number of words in the text: 6,414 25 26 List of all elements of the manuscript: Main text, 1 Table, 5 Figures, 27 Supplementary Material 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434967; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 28 ABSTRACT: Intergenerational effects, also known as parental effects in which the 29 offspring phenotype is influenced by the parental phenotype, can occur in response 30 to factors that occur not only in early but also in late parental life. However, little is 31 known about how these parental life stage-specific environments interact with each 32 other and with the offspring environment to influence offspring phenotype, particularly 33 in organisms that realize distinct niches across ontogeny. We examined the effects of 34 parental larval starvation and adult reproductive environment on offspring traits under 35 matching or mismatching offspring larval starvation conditions using the 36 holometabolous, haplo-diploid insect Athalia rosae (turnip sawfly). We show that the 37 parental larval starvation treatment had trait-dependent intergenerational effects on 38 both life-history and consumption traits of offspring larvae, partly in interaction with 39 offspring conditions and sex, while there was no significant effect of parental adult 40 reproductive environment. In addition, while offspring larval starvation led to 41 numerous gene- and pathway-level expression differences, parental larval starvation 42 impacted fewer genes and only the ribosomal pathway. Our findings reveal that 43 parental starvation evokes complex intergenerational effects on offspring life-history 44 traits, consumption patterns as well as gene expression, although the effects are less 45 pronounced than those of offspring starvation. 46 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434967; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 47 Introduction 48 Intergenerational effects, more commonly known as parental effects, are defined as 49 causal influences of parental phenotype on offspring phenotype, likely mediated by 50 non-DNA sequence-based inheritance (Wolf and Wade 2009; Perez and Lehner 51 2019). Together with transgenerational effects, which occur across several 52 generations, they play a key role in the ecology and evolution of organisms (Badyaev 53 and Uller 2009) and impact the responses of individuals to changing environmental 54 conditions (Sánchez-Tójar et al. 2020). One important environmental factor that can 55 rapidly change during an organism’s lifetime and across generations is food 56 availability. Periods of starvation are commonly encountered by insects in the wild 57 (Jiang et al. 2019) and, when experienced early in life, often have long-lasting 58 consequences on an individual’s phenotype (Miyatake 2001; Wang et al. 2016; 59 McCue et al. 2017) and the phenotype of the offspring (Saastamoinen et al. 2013; 60 McCue et al. 2017; Paul et al. 2019). However, it is also becoming increasingly 61 apparent that to fully elucidate the adaptive nature of intergenerational effects, 62 studies should encompass different phases in development of the parental life cycle 63 and how such life stage-specific experience affects offspring phenotype (English and 64 Barreaux 2020). 65 The conditions experienced particularly during two phases of parental life, early life 66 and later life during mating and reproduction, can have lasting, sometimes 67 irreversible impacts on development trajectories of offspring (Monaghan 2008; Burton 68 and Metcalfe 2014; Taborsky 2017). A favorable environment experienced in early 69 life may result in better conditioned offspring (van de Pol et al. 2006) that can better 70 cope with stress (Franzke and Reinhold 2013). This is often called silver spoon or 71 carry-over effect (Monaghan 2008). Negative effects of a poor start in life might also 72 be passed on, resulting in offspring less able to cope with stressful conditions 73 (Naguib et al. 2006). Alternatively, such stressed individuals may produce offspring 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434967; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 74 that are buffered against stressors, for example, through parental provisioning 75 (Valtonen et al. 2012; Pilakouta et al. 2015; Hibshman et al. 2016). Finally, 76 regardless of how favorable conditions are, it may be most important that they match 77 between parents and offspring. Evidence for such predictive adaptive effects has 78 been found in several species (Raveh et al. 2016; Le Roy et al. 2017), but is weak in 79 others (Uller et al. 2013). Each of these trajectories of intergenerational effects are 80 not mutually exclusive. For example, offspring in mismatched environments may do 81 relatively better if their parents were of high quality, due to silver spoon effects 82 (Engqvist and Reinhold 2016). Furthermore changes in parental investment based on 83 mate cues (Cunningham and Russell 2000; Cornwallis and O'Connor 2009) may 84 potentially counteract or augment the effects of the parental early life environment on 85 offspring phenotype. As niches often shift across an individual’s lifetime, both 86 parental early and later life environments and their interaction must be considered as 87 factors that can influence offspring phenotypes. 88 With discrete phases during development, insects, particularly holometabolous 89 insects, present ideal organisms in which to investigate how environmental cues 90 experienced during early life but also during adulthood (e.g. mating) may interact with 91 offspring environment, to influence individual offspring phenotypes (English and 92 Barreaux 2020). Periods of larval starvation are known to influence developmental 93 trajectories with knock-on effects on adult size, reproductive success and adult 94 starvation resistance (Boggs and Niitepõld 2016; Wang et al. 2016). Individuals may 95 respond to periods of starvation with increased food uptake (Regalado et al. 2017) as 96 well as compensatory growth (i.e. a faster growth rate) or catch-up growth (i.e. 97 attaining a minimum size by prolonging the larval development) (Hector and 98 Nakagawa 2012). Moreover, starvation leads to substantial shifts in gene expression 99 (Moskalev et al. 2015; Jiang et al. 2019; Etebari et al. 2020; Farahani et al. 2020). 100 However, little is known about how long these effects may persist (McCue et al. 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434967; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 101 2017) and to what extent parental starvation may affect gene expression of offspring 102 experiencing matching or mismatching conditions. 103 In the present study, we investigated the effects of parental larval starvation and 104 parental reproductive environment on offspring (i.e. intergenerational effects), under 105 matching or mismatching larval starvation conditions, using the turnip sawfly, Athalia 106 rosae (Hymenoptera: Tenthredinidae). The larvae feed on leaves of various species 107 of Brassicaceae, including crops, and can readily experience periods of starvation 108 when their hosts are overexploited (Riggert 1939). The adults are nectar-feeding and 109 in addition collect neo-clerodanoid-like compounds (hereafter called ‘clerodanoids’) 110 from non-Brassicaceae plants. Clerodanoid-uptake improves their mating probability 111 (Amano et al. 1999) and affects interactions between and within sexes (preprint Paul 112 et al. 2021; preprint Paul and Müller 2021). This behavior is thus an important aspect 113 of the adult life-history, but potential influences on offspring life-history traits have, to 114 our knowledge, not yet been studied. We measured key life-history traits (i.e., 115 developmental time and adult body mass) to assess the combined
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