DOI: 10.5061/dryad.bzkh189dr
title: Early-life food stress hits females harder than males in insects: a meta-analysis of sex differences in environmental sensitivity

description: Fitness consequences of early-life environmental conditions are often
 sex-specific, but corresponding evidence for invertebrates remains
 inconclusive. Here we use meta-analysis to evaluate sex-specific
 sensitivity to early-life nutritional conditions in insects. Using
 literature-derived data for 85 species with broad phylogenetic and
 ecological coverage, we show that females are generally more sensitive to
 food stress than males. Stressful nutritional conditions during
 development typically lead to female-biased mortality and thus
 increasingly male-biased sex ratios of emerging adults. We further
 demonstrate that the general trend of higher sensitivity to food stress in
 females can primarily be attributed to their typically larger body size in
 insects and hence higher energy needs during development. By contrast,
 there is no consistent evidence of sex-biased sensitivity in sexually
 size-monomorphic species. Drawing conclusions regarding sex-biased
 sensitivity in species with male-biased size dimorphism remains to wait
 for the accumulation of relevant data. Our results suggest that
 environmental conditions leading to elevated juvenile mortality may
 potentially affect the performance of insect populations further by
 reducing the proportion of females among individuals reaching reproductive
 age. Accounting for sex-biased mortality is therefore essential to
 understanding the dynamics and demography of insect populations, not least
 importantly in the context of ongoing insect declines.
description: <strong>Data
 collection</strong> These data were collected for a meta-analysis to
 assess sex-specific sensitivity to early-life nutritional conditions in
 insects. We made use of
 experimental case studies reporting sex ratios at adult emergence in
 conspecifics reared under two or more diet treatments (food quality or
 availability). We collated primary studies in two complementary ways. The
 majority of primary data sets for this synthesis were collected
 systematically by the lead author (T. Teder) from an extensive list of
 journals in the field of entomology, ecology and evolutionary biology,
 partly as a result of one-time retrospective screening (articles published
 before 2003) and partly as a result of continuous screening (articles
 published between 2004 and 2021) of journals' tables of contents. Our
 systematic screening meant that the journals' tables of contents were
 routinely examined, and all papers identified as potentially containing
 relevant data on the basis of article titles were subjected to full-text
 review. As data of this type are typically reported in tables and figures,
 their identification within articles was straightforward.
 To
 increase the amount of primary data, additional studies were identified by
 a thorough search in major literature databases (Google Scholar, Web of
 Science, Scopus, published until 2021). These complementary searches in
 the literature databases were undertaken to find relevant data in journals
 that remained uncovered by our main data collection method. Accordingly,
 while exploring the search results, we primarily focused on studies
 published in journals that were not subjected to systematic screening. The
 basic procedure for identifying relevant primary papers among search
 results was basically identical to that used when screening journals'
 contents: papers identified as potentially containing relevant data based
 on article titles were retrieved for full-text review. To minimize any
 search-related biases, we used only search queries that were strictly
 neutral concerning the focal questions of our study (i.e. sex-specific
 sensitivity to nutritional stress). Accordingly, our search queries
 included only combinations of very generic search terms: one of several
 synonyms of sex ratio ('sex ratio',
 'proportion/percentage/fraction of males/females'),
 'mortality' and one of particular insect order names
 ('Diptera', 'Hemiptera', 'Lepidoptera',
 'Coleoptera', 'Orthoptera', etc., or
 'insect*'). No restriction was set on the language or
 publication year of primary studies. 
 As a major exception, we
 systematically ignored studies focusing on Hymenoptera and Thysanoptera
 during the process of data collection. These groups of insects have
 haplodiploid sex determination (males develop from unfertilized and
 females from fertilized eggs) which provides mothers with an efficient
 mechanism for manipulating offspring sex ratio. We also did not consider
 taxa regularly exhibiting asexual reproduction, such as
 aphids. <strong>Data extraction and criteria for
 eligibility</strong> For a study to be considered, it had to provide
 two types of information: i) sex ratios at adult emergence for multiple
 (two or more) diet treatments together with sample sizes, and ii)
 corresponding juvenile mortality rates. Typically, sex ratios in primary
 studies were reported as the proportion/percentage of males/females or the
 ratio of the two sexes at adult emergence (or, in a few cases, at the
 pupal stage). As sample sizes for sex ratio estimates were not always
 explicitly indicated, we applied various indirect approaches to derive
 them, most often combining information on sample sizes at the start of the
 experiment with data on mortality throughout juvenile stages.
 The
 combined juvenile mortality rate of the two sexes was used as a proxy for
 nutritional stress. Accordingly, our research relies on the premise that,
 within each primary study, food stress was most severe in treatments with
 the highest mortality rates and least pronounced in treatments with the
 lowest mortality rates. Both egg-to-adult and larval mortality rates
 (often reported as survival rates) were considered equally acceptable
 measures of juvenile mortality. In a few cases, we also accepted mortality
 rates estimated over a particular fixed part of the larval stage (two
 primary studies) or the pupal stage (three studies).
 We
 limited our inclusion criteria to studies where major external mortality
 agents – predators and parasitoids – were explicitly excluded. In all
 studies included, experimental treatments were applied to the F1
 generation only, whereas their parents were maintained under identical
 conditions, excluding in this way any parental effect on sex
 ratios.
 Among-treatment
 differences in nutritional stress were solely due to variations in food
 quality (e.g., different host plants, different prey species, also
 different artificial diets) or food availability. Otherwise, the
 conditions were uniform within the experiments. Data from multifactorial
 experiments (e.g. those manipulating both diet and temperature) were
 divided into different data sets so that the environmental factor of our
 interest was allowed to vary while other factors were held constant. In
 some primary studies, food quality and amount were manipulated
 indistinguishably within the same experimental setup. Data extracted from
 different studies were always treated as different data sets. However,
 data from a single study could also be split into multiple primary data
 sets if obtained from different experiments or using different
 species/populations/genotypes. We deliberately did not consider studies in
 which diet treatments applied contained pesticides or their residues.
 WebPlotDigitizer 4.3 (A. Rohatgi; https://automeris.io/WebPlotDigitizer) was used to extract graphically presented data. One should note that the overwhelming majority of primary studies were conducted in contexts other than the focus of our synthesis: sex differences in stress responses per se were rarely addressed in these papers. Therefore, a considerable share of primary studies found, between-treatment differences in juvenile mortality were relatively small, indicating low variation in environmental stress levels. Naturally, in order to meaningfully evaluate sex-specific responses to food stress, there must be some variation in food stress across treatments. We therefore arbitrarily limited our main database to a subset of primary studies in which mortality rates across treatments had at least a 10 % difference (calculated as the difference between the maximum and minimum mortality rates across treatments). This way we ensured that growth conditions within studies were not "too similar" across treatments. Applying this threshold retained us altogether 125 primary data sets which formed the backbone of our analyses.
description: Data are provided as .xlsx files, and R scripts are provided for
 analyses. We encourage researchers interested in the re-use of this data
 set and code to contact the authors of the data set.