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

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).

Sex differences in spiders: from phenotype to genomics

“…Particularly in species with a large sexual size dimorphism, males are affected most strongly by food restriction during early life, while females are generally able to compensate early restrictions if conditions improve later in life. Studies in Trichonephila senegalensis have shown that females delay maturation and reach the body size of sisters that were raised under high food conditions (Neumann et al 2017). Body size and body condition are generally good predictors for fecundity in spiders (Head 1995), and current knowledge supports that females optimize body size if necessary, at the cost of delayed maturation.…”

“…Evidence is increasing that both instar number and instar duration are plastic traits in both sexes and respond to external conditions such as prey availability and quality, daylength, temperature, and even social cues. Growth studies have shown that females and males respond differently to variation in diet (Neumann et al 2017;Uhl et al 2004) suggesting sex-dependent growth strategies and divergent selection pressures on male and female lifehistory traits (Kleinteich and Schneider 2010;Uhl et al 2004). Particularly in species with a large sexual size dimorphism, males are affected most strongly by food restriction during early life, while females are generally able to compensate early restrictions if conditions improve later in life.…”

Guiding lights: Foraging responses of juvenile nocturnal orb‐web spiders to the presence of artificial light at night

“…However, it is unclear whether the association between the presence of artificial light and prey capture success that spiders prioritise illumination over prey availability as cues for web site tenacity. Comparatively, little is known about the foraging strategies of juvenile spiders, despite the impact of juvenile foraging on adult size and rates of development (Moya-Laraño, Orta-Ocaña, Barrientos, Bach, & Wise, 2003;Neumann, Ruppel, & Schneider, ), although they appear to be less resistant to moving their webs (Chmiel et al, 2000;Enders, 1975).…”

“…Exposure to ALAN stimulates faster maturation but a smaller adult size in E. biapicata when diet is controlled (Willmott, Henneken, Selleck, & Jones, 2018). Maturation rate and eventual body size both depend on juvenile foraging success (Moya-Laraño et al, 2003;Neumann et al, ), so a more complete understanding of the impacts of ALAN on these spiders requires a comparison of the prey capture rates of juvenile spiders in illuminated and naturally dark sites.…”

Two sexes respond equally to food restriction in a sexually dimorphic but not body mass dimorphic jumping spider

“…These adaptive strategies not only differ among species, but also within species (Cordellier et al, 2020;Leimar et al, 1994;Neumann et al, 2017;Nylin & Gotthard, 1998;Uhl et al, 2004). Understanding the intraspecific differences in adaptive strategies under food restriction might help us understand how selection shapes the intersexual or inter-age differences.…”