Abstract
Adult body size, development time, and growth rates are components of organismal life histories, which crucially influence fitness and are subject to trade-offs. If selection is sex-specific, male and female developments can eventually lead to different optimal sizes. This can be achieved through developmental plasticity and sex-specific developmental trajectories. Spiders present suitable animals to study differences in developmental plasticity and life history trade-offs between the sexes, because of their pronounced sexual dimorphism. Here, we examine variation in life histories in the extremely sexually size dimorphic African hermit spider (Nephilingis cruentata) reared under standardized laboratory conditions. Females average 70 times greater body mass (and greater body size) at maturity than males, which they achieve by developing longer and growing faster. We find a small to moderate amount of variability in life history traits to be caused by family effects, comprising genetic, maternal, and early common environmental effects, suggesting considerable plasticity in life histories. Remarkably, family effects explain a higher variance in male compared to female life histories, implying that female developmental trajectories may be more responsive to environment. We also find sex differences in life history trade-offs and show that males with longer development times grow larger but exhibit shorter adult longevity. Female developmental time also correlates positively with adult body mass, but the trade-offs between female adult mass, reproduction, and longevity are less clear. We discuss the implications of these findings in the light of evolutionary trade-offs between life history traits.
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References
Andrade MCB (2019) Sexual selection and social context: web-building spiders as emerging models for adaptive plasticity. In: Advances in the study of behavior, 1st edn., Vol. 51. Elsevier Inc., pp 177–250. https://doi.org/10.1016/bs.asb.2019.02.002
Bates D, Mächelr M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1). https://doi.org/10.18637/jss.v067.i01
Bernardo J (1996) Maternal effects in animal ecology. Amer Zool 36:83–105. https://doi.org/10.1093/icb/36.2.83
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75(4):385–407. https://doi.org/10.1086/393620
Bonduriansky R (2007) The evolution of condition-dependent sexual dimorphism. Am Nat 169(1):9–19. https://doi.org/10.1086/510214
Chapman T, Miyatake T, Smith HK, Partridge L (1998) Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc R Soc Lond Biol 265(1408):1879–1894. https://doi.org/10.1098/rspb.1998.0516
Christenson TE, Goist KC (1979) Costs and benefits of male : male competition in the orb weaving spider, NephilaClavipes. Behav Ecol Sociobiol 5(1):87–92
Corcobado G, Rodríguez-Gironés MA, De Mas E, Moya-Laraño J (2010) Introducing the refined gravity hypothesis of extreme sexual size dimorphism. BMC Evol Biol 10:236. https://doi.org/10.1186/1471-2148-10-236
Cordellier M, Schneider JM, Uhl G, Posnien N (2020) Sex differences in spiders: from phenotype to genomics. Dev Genes Evol 230(2):155–172. https://doi.org/10.1007/s00427-020-00657-6
Cory AL, Schneider JM (2018) Mate availability does not influence mating strategies in males of the sexually cannibalistic spider Argiope bruennichi. PeerJ 6:e5360. https://doi.org/10.7717/peerj.5360
Elgar MA, Schneider JM, Herberstein ME (2000) Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc R Soc Lond Biol 267(1460):2439–2443. https://doi.org/10.1098/rspb.2000.1303
Esperk T, Tammaru T, Nylin S (2007) Intraspecific variability in number of larval instars in insects. J Econ Entomol 100(3):627–645. https://doi.org/10.1603/0022-0493(2007)100[627:IVINOL]2.0.CO;2
Fairbairn DJ (2005) Allometry for sexual size dimorphism: testing two hypotheses for Rensch’s rule in the water strider Aquarius remigis. Am Nat 166(4):69–84. https://doi.org/10.1086/444600
Fernández-Montraveta C, Moya-Laraño J (2007) Sex-specific plasticity of growth and maturation size in a spider: implications for sexual size dimorphism. J Evol Biol 20(5):1689–1699. https://doi.org/10.1111/j.1420-9101.2007.01399.x
Foelix RF (2011) Biology of Spiders. Insect Syst Evol 14(1):1–16. https://doi.org/10.1163/187631283X00371
Foellmer MW, Fairbairn DJ (2005) Competing dwarf males: sexual selection in an orb-weaving spider. J Evol Biol 18(3):629–641. https://doi.org/10.1111/j.1420-9101.2005.00868.x
Foellmer MW, Moya-Laraño J (2007) Sexual size dimorphism in spiders: patterns and processes. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism, Oxford Scholarship Online, pp 71–82. https://doi.org/10.1093/acprof:oso/9780199208784.003.0008
Gilburn AS, Day TH (1994) Sexual dimorphism, sexual selection and the αβ chromosomal inversion polymorphism in the seaweed fly, Coelopa frigida. Proc R Soc Lond Biol 257(1350):303–309. https://doi.org/10.1098/rspb.1994.0130
Head G (1995) Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (class Araneae). Evol 49(4):776–781. https://doi.org/10.2307/2410330
Higgins L (2000) The interaction of season length and development time alters size at maturity. Oecologia 122(1):51–59. https://doi.org/10.1007/PL00008835
Higgins L, Coddington J, Goodnight C, Kuntner M (2011) Testing ecological and developmental hypotheses of mean and variation in adult size in nephilid orb-weaving spiders. Evol Ecol 25(6):1289–1306. https://doi.org/10.1007/s10682-011-9475-9
Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492. https://doi.org/10.2307/3544943
Kasumovic MM, Andrade MCB (2009) A change in competitive context reverses sexual selection on male size. J Evol Biol 22(2):324–333. https://doi.org/10.1111/j.1420-9101.2008.01648.x
Kasumovic MM, Brooks RC (2011) It’s all who you know : the evolution of socially cued anticipatory plasticity as a mating strategy. Q Rev Biol 86(3):181–197
Kleinteich A, Schneider JM (2011) Developmental strategies in an invasive spider: constraints and plasticity. Ecol Entomol 36(1):82–93. https://doi.org/10.1111/j.1365-2311.2010.01249.x
Kralj-Fišer S, Gregorič M, Zhang S, Li D, Kuntner M (2011) Eunuchs are better fighters. Anim Behav 81(5):933–939. https://doi.org/10.1016/j.anbehav.2011.02.010
Kralj-Fišer S, Kuntner M (2012) Eunuchs as better fighters? Sci Nat 99(2):95–101
Kralj-Fišer S, Sanguino Mostajo GA, Preik O, Pekár S, Schneider JM (2013) Assortative mating by aggressiveness type in orb weaving spiders. Behav Ecol 24(4):824–831. https://doi.org/10.1093/beheco/art030
Kralj-Fišer S, Čelik T, Lokovšek T, Šuen K, Šiling R, Kuntner M (2014) Development and growth in synanthropic species: plasticity and constraints. Sci Nat 101(7):565–575. https://doi.org/10.1007/s00114-014-1194-y
Kralj-Fišer S, Čandek K, Lokovšek T, Čelik T, Cheng R-C, Elgar MA, Kuntner M (2016) Mate choice and sexual size dimorphism, not personality, explain female aggression and sexual cannibalism in raft spiders. Anim Behav 111https://doi.org/10.1016/j.anbehav.2015.10.013
Kuntner M (2007) A monograph of Nephilengys, the pantropical “hermit spiders” (Araneae, Nephilidae, Nephilinae). Syst Entomol 32(1). https://doi.org/10.1111/j.1365-3113.2006.00348.x
Kuntner M, Gregorič M, Zhang S, Kralj-Fišer S, Li D (2012) Mating plugs in polyandrous giants: Which sex produces them, when, how and why? PLoS ONE 7(7). https://doi.org/10.1371/journal.pone.0040939
Kuntner M, Coddington JA (2020) Sexual size dimorphism: evolution and perils of extreme phenotypes in spiders. Ann Rev Entomol 65:57–80. https://doi.org/10.1146/annurev-ento-011019-025032
Lee QQ, Oh J, Kralj-Fišer S, Kuntner M, Li D (2012) Emasculation: gloves-off strategy enhances eunuch spider endurance. Biol Lett 8(5):733–735. https://doi.org/10.1098/rsbl.2012.0285
Leimar O (1996) Life history plasticity : influence of photoperiod on growth and development in the common blue butterfly. Oikos 76(2):228–234. https://doi.org/10.2307/3546194
Li D, Jackson RR (1996) How temperature affects development and reproduction in spiders: a review. J Therm Biol 21(4):245–274. https://doi.org/10.1016/0306-4565(96)00009-5
Lissowsky N, Kralj-Fišer S, Schneider JM (2021) Giant and dwarf females: how to explain the fourfold variation in body size and fecundity in Trichonephilasenegalensis (Aranea: Nephilidae). Biol J Linn Soc 2021:blab059. https://doi.org/10.1093/biolinnean/blab059
Lovich JE, Gibbons JW (1992) Review of techniques for quantifying sexual size dimorphism. Growth Dev Aging 56(4):269–281
Miyashita K, Department (1987) Development and egg sac production of Achaearanea tepidariorum (C. L. Koch) (Araneae, Theridiidae) under long and short photoperiods. J Arachnol 15(1):51–58
Moore MP, Whiteman HH, Martin RA (2019) A mother’s legacy: the strength of maternal effects in animal populations. Ecol Lett 22(10):1620–1628. https://doi.org/10.1111/ele.13351
Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Ann Rev Entomol 36(1):511–534. https://doi.org/10.1146/annurev.en.36.010191.002455
Neumann R, Schneider JM (2015) Differential investment and size-related mating strategies facilitate extreme size variation in contesting male spiders. Anim Behav 101:107–115. https://doi.org/10.1016/j.anbehav.2014.12.027
Neumann R, Schneider JM (2016) Socially cued developmental plasticity in web-building spiders. BMC Evol Biol 16(1):1–9. https://doi.org/10.1186/s12862-016-0736-7
Neumann R, Ruppel N, Schneider JM (2017) Fitness implications of sex-specific catch-up growth in Nephila senegalensis, a spider with extreme reversed SSD. PeerJ 2017(11). https://doi.org/10.7717/peerj.4050
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Ann Rev Entomol 43:63–83. https://doi.org/10.1146/annurev.ento.43.1.63
Partridge L, Sibly R (1991) Constraints in the evolution of life histories. Philos Trans R Soc Lond B Biol Sci 332(1262):3–13. https://doi.org/10.1098/rstb.1991.0027
Quiñones-Lebrón SG, Gregorič M, Kuntner M, Kralj-Fišer S (2019) Small size does not confer male agility advantages in a sexually-size dimorphic spider. PLoS ONE 14(5). https://doi.org/10.1371/journal.pone.0216036
Quiñones-Lebrón SG, Kuntner M, Kralj-Fišer S (2021) The effect of genetics, diet, and social environment on adult male size in a sexually dimorphic spider. Evol Ecol 35(2):217–234. https://doi.org/10.1007/s10682-020-10097-3
R Development Core Team (2019) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
Roff D (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York
Roff D (2012) Evolutionary quantitative genetics. Springer Science & Business Media, B.V.
Schaefer M (1977) Winter ecology of spiders (Araneida). Zeitschrift Für Angew Entomol 83(1–4):113–134. https://doi.org/10.1111/j.1439-0418.1977.tb02381.x
Scharf I, Peter F, Martin OY (2013) Reproductive trade-offs and direct costs for males in arthropods. Evol B 40(2):169–184. https://doi.org/10.1007/s11692-012-9213-4
Schneider JM, Elgar MA (2000) Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes (Araneoidea): female and male perspectives. Behav Ecol 12(5):547–552. https://doi.org/10.1093/beheco/12.5.547
Singer MC (1982) Sexual selection for small size in male butterflies. Am Nat 119(3):440–443
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stillwell RC, Fox CW (2009) Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity. Oikos 118(5):703–712. https://doi.org/10.1111/j.1600-0706.2008.17327.x
Stillwell RC, Blanckenhorn WU, Teder T, Davidowitz G, Fox CW (2010) Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Ann Rev Entomol 55:227–245. https://doi.org/10.1146/annurev-ento-112408-085500.Sex
Tammaru T, Kaitaniemi P, Ruohomaki K (1996) Realized fecundity in Epirrita autumnata (Lepidoptera: Geometridae): relation to body size and consequences to population dynamics. Oikos 77(3):407–416. https://doi.org/10.2307/3545931
Turk E, Kuntner M, Kralj-Fišer S (2018) Cross-sex genetic correlation does not extend to sexual size dimorphism in spiders. Sci Nat105https://doi.org/10.1007/s00114-017-1529-6
Uetz GW (1992) Foraging strategies of spiders. Trends Ecol Evol 7(5):155–159. https://doi.org/10.1016/0169-5347(92)90209-T
Uhl G, Schmitt S, Schäfer MA, Blanckenhorn W (2004) Food and sex-specific growth strategies in a spider. Evol Ecol Res 6(4):523–540. https://doi.org/10.5167/uzh-172731
Vollrath F (1987) Foraging, growth and reproductive success. In: Nentwig W (ed) Ecophysiology of spiders. Springer, Berlin Heidelberg New York, pp 357–370
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
Zonneveld C (1996) Being big or emerging early? Polyandry and the trade-off between size and emergence in male butterflies. Am Nat 147(6):946–965
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The authors were supported by the Slovenian Research Agency (grants P1-0236, P1-0255, J1-9163).
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Conceptualization, ideas and formulation or evolution of overarching research goals and aims: Simona Kralj-Fišer (SKF).
Field work and specimen acquisition: Matjaž Kuntner (MK), Charles R. Haddad (CRH), Matjaž Gregorič (MG), Tjaša Lokovšek (TL), Klemen Čandek (KČ), and Shakira Quinones (SQ).
Animal rearing: lead, Rok Golobinek (RG); equal, TL, Eva Turk (ET), Janko Šet (JŠ), and SKF; support, MG and SQ.
Data curation, management activities to annotate (produce metadata), scrub data, and maintain research data (including software code, where it is necessary for interpreting the data itself) for initial use and later re-use: RG, JŠ, TL, and SKF.
Formal analysis, application of statistical, mathematical, computational, or other formal techniques to analyse or synthesize study data: ET.
Funding acquisition, acquisition of the financial support for the project leading to this publication: SKF and MK.
Investigation, conducting a research and investigation process, specifically performing the experiments, or data/evidence collection: lead, SKF; equal, RG, ET, JŠ, and TL.
Methodology, development or design of methodology, and creation of models: SKF and ET.
Project administration, management, and coordination responsibility for the research activity planning and execution: SKF.
Supervision, oversight and leadership responsibility for the research activity planning and execution, including mentorship external to the core team: SKF.
Validation, verification, whether as a part of the activity or separate, of the overall replication/reproducibility of results/experiments and other research outputs: SKF.
Visualization, preparation, creation, and/or presentation of the published work, specifically visualization/data presentation: ET (graphs, tables) and MG (photo).
Writing — original draft, preparation, creation, and/or presentation of the published work, specifically writing the initial draft (including substantive translation): SKF, ET, and JŠ.
Writing — review and editing: JŠ, ET, RG, TL, MG, SQ, CRH, KČ, MK, and SKF.
Preparation, creation, and/or presentation of the published work by those from the original research group, specifically critical review, commentary, or revision, including pre- or post-publication stages: SKF.
Revision: ET and SKF.
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Research on spiders is not restricted by the animal welfare law of the country where the study was conducted. In the field, we collected the minimum number of individuals needed to conduct the research. The spiders were kept in conditions similar to their natural environmental conditions. The spiders were regularly fed with different prey items. The study was non-invasive. After the experiments, the spiders remained in the laboratory and were reared until natural death, as described above.
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Janko Šet, and Eva Turk contributed equally to this work
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Šet, J., Turk, E., Golobinek, R. et al. Sex-specific developmental trajectories in an extremely sexually size dimorphic spider. Sci Nat 108, 54 (2021). https://doi.org/10.1007/s00114-021-01754-w
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DOI: https://doi.org/10.1007/s00114-021-01754-w