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 stag...

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Main Authors: Rainer Neumann, Nicole Ruppel, Jutta M. Schneider
Format: Article
Language:English
Published: PeerJ Inc. 2017-11-01
Series:PeerJ
Subjects:
SSD
Online Access:https://peerj.com/articles/4050.pdf
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spelling doaj-850a12762bb44369b48b8f3b693c625d2020-11-24T20:56:58ZengPeerJ Inc.PeerJ2167-83592017-11-015e405010.7717/peerj.4050Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSDRainer Neumann0Nicole Ruppel1Jutta M. Schneider2Zoologisches Institut, Biozentrum Grindel, Universität Hamburg, Hamburg, GermanyZoologisches Institut, Biozentrum Grindel, Universität Hamburg, Hamburg, GermanyZoologisches Institut, Biozentrum Grindel, Universität Hamburg, Hamburg, GermanyBackground 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).https://peerj.com/articles/4050.pdfCompensatory growthSSDDevelopmental plasticityLife-historyFeeding conditionsAraneae
collection DOAJ
language English
format Article
sources DOAJ
author Rainer Neumann
Nicole Ruppel
Jutta M. Schneider
spellingShingle Rainer Neumann
Nicole Ruppel
Jutta M. Schneider
Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
PeerJ
Compensatory growth
SSD
Developmental plasticity
Life-history
Feeding conditions
Araneae
author_facet Rainer Neumann
Nicole Ruppel
Jutta M. Schneider
author_sort Rainer Neumann
title Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
title_short Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
title_full Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
title_fullStr Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
title_full_unstemmed Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD
title_sort fitness implications of sex-specific catch-up growth in nephila senegalensis, a spider with extreme reversed ssd
publisher PeerJ Inc.
series PeerJ
issn 2167-8359
publishDate 2017-11-01
description 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).
topic Compensatory growth
SSD
Developmental plasticity
Life-history
Feeding conditions
Araneae
url https://peerj.com/articles/4050.pdf
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