Abstract

BackgroundAnimal growth is often constrained by unfavourable conditions and divergences from optimal body size can be detrimental to an individual’s fitness, particularly in species with determinate growth and a narrow time-frame for life-time reproduction. Growth restriction in early juvenile stages can later be compensated by means of plastic developmental responses, such as adaptive catch-up growth (the compensation of growth deficits through delayed development). Although sex differences regarding the mode and degree of growth compensation have been coherently predicted from sex-specific fitness payoffs, inconsistent results imply a need for further research. We used the African Nephila senegalensis, representing an extreme case of female-biased sexual size dimorphism (SSD), to study fitness implications of sex-specific growth compensation. We predicted effective catch-up growth in early food-restricted females to result in full compensation of growth deficits and a life-time fecundity (LTF) equivalent to unrestricted females. Based on a stronger trade-off between size-related benefits and costs of a delayed maturation, we expected less effective catch-up growth in males.MethodsWe tracked the development of over one thousand spiders in different feeding treatments, e.g., comprising a fixed period of early low feeding conditions followed by unrestricted feeding conditions, permanent unrestricted feeding conditions, or permanent low feeding conditions as a control. In a second experimental section, we assessed female fitness by measuring LTF in a subset of females. In addition, we tested whether compensatory development affected the reproductive lifespan in both sexes and analysed genotype-by-treatment interactions as a potential cause of variation in life-history traits.ResultsBoth sexes delayed maturation to counteract early growth restriction, but only females achieved full compensation of adult body size. Female catch-up growth resulted in equivalent LTF compared to unrestricted females. We found significant interactions between experimental treatments and sex as well as between treatments and family lineage, suggesting that family-specific responses contribute to the unusually large variation of life-history traits in Nephila spiders. Our feeding treatments had no effect on the reproductive lifespan in either sex.DiscussionOur findings are in line with predictions of life-history theory and corroborate strong fecundity selection to result in full female growth compensation. Males showed incomplete growth compensation despite a delayed development, indicating relaxed selection on large size and a stronger trade-off between late maturation and size-related benefits. We suggest that moderate catch-up growth in males is still adaptive as a ‘bet-hedging’ strategy to disperse unavoidable costs between life-history traits affected by early growth restriction (the duration of development and adult size).

Highlights

  • Body size and the duration of development are among the most fitness-relevant life-history traits and have been extensively studied in various animal taxa

  • As large males tend to succeed in male-male competition across animal taxa, body size in males is often subject to sexual selection, resulting in male-biased sexual size dimorphism (SSD) (Kingsolver & Pfennig, 2004)

  • Mortality rates during the first four weeks of the experiment did not differ significantly between early treatments; 59 of 626 spiders died under high feeding conditions (9.4%) and 74 of 630 spiders died under low feeding conditions (11.8%) (G-test: χ 2 = 1.79, P = 0.18; N = 1256). (Sex-determination is impossible in small juvenile spiders; mortality rates were analysed independent of sex.)

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Summary

Introduction

Body size and the duration of development are among the most fitness-relevant life-history traits and have been extensively studied in various animal taxa (reviewed in Blanckenhorn, 2005; Nylin & Gotthard, 1998; Roff, 2002). We predicted effective catch-up growth in early food-restricted females to result in full compensation of growth deficits and a life-time fecundity (LTF) equivalent to unrestricted females. Both sexes delayed maturation to counteract early growth restriction, but only females achieved full compensation of adult body size. Males showed incomplete growth compensation despite a delayed development, indicating relaxed selection on large size and a stronger trade-off between late maturation and sizerelated benefits. We suggest that moderate catch-up growth in males is still adaptive as

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