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

Abstract

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).

Keywords: Araneae; Araneidae; Compensatory growth; Developmental plasticity; Feeding conditions; Life-history; SSD.

Figure 1. Adaptive catch-up growth in (A) male and (B) female Nephila senegalensis.

Symbols indicate median values for body mass at the beginning of the late-experiment development and body mass at sexual maturation in treatments High-High (blue squares) and Low-High (red triangles). Late-experiment development in the High-High treatment followed four weeks of early high feeding conditions. Late-experiment development in the Low-High treatment followed four weeks of early low feeding conditions. Body mass is given as a proxy of body size (*, indicates significant differences).

Figure 2. Effects of feeding treatments on the duration of development and adult size in Nephila senegalensis.

Top row (A, B): Males. Bottom row (C, D): Females. Treatments were High-High (H-H), Low-Low (L-L), High-Low (H-L), and Low-High (L-H).

Figure 3. Effects of feeding treatments on life-time fecundity (LTF) in Nephila senegalensis.

The interaction between Treatment and the number of clutches produced explained life-time fecundity in a linear model (adjusted R² = 0.83). Treatments were High-High (blue), Low-High (red), and Low-Low (green). Shaded areas indicate 95% confidence intervals.