Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD

BACKGROUND: Animal 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. METHODS: We 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. RESULTS: Both 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. DISCUSSION: Our 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).