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Oecologia

, Volume 191, Issue 1, pp 61–71 | Cite as

Ecophysiological determinants of sexual size dimorphism: integrating growth trajectories, environmental conditions, and metabolic rates

  • Marie-Claire CheliniEmail author
  • John P. Delong
  • Eileen A. Hebets
Physiological ecology – original research

Abstract

Sexual size dimorphism (SSD) often results in dramatic differences in body size between females and males. Despite its ecological importance, little is known about the relationship between developmental, physiological, and energetic mechanisms underlying SSD. We take an integrative approach to understand the relationship between developmental trajectories, metabolism, and environmental conditions resulting in extreme female-biased SSD in the crab spider Mecaphesa celer (Thomisidae). We tested for sexual differences in growth trajectories, as well as in the energetics of growth, hypothesizing that female M. celer have lower metabolic rates than males or higher energy assimilation. We also hypothesized that the environment in which spiderlings develop influences the degree of SSD of a population. We tracked growth and resting metabolic rates of female and male spiderlings throughout their ontogeny and quantified the adult size of individuals raised in a combination of two diet and two temperature treatments. We show that M. celer’s SSD results from differences in the shape of female and male growth trajectories. While female and male resting metabolic rates did not differ, diet, temperature, and their interaction influenced body size through an interactive effect with sex, with females being more sensitive to the environment than males. We demonstrate that the shape of the growth curve is an important but often overlooked determinant of SSD and that females may achieve larger sizes through a combination of high food ingestion and low activity levels. Our results highlight the need for new models of SSD based on ontogeny, ecology, and behavior.

Keywords

Growth trajectories Ontogeny SSD Temperature-size rule Thomisidae 

Notes

Acknowledgements

D. Izaguirre, D. Myers, M. Potts, A. Schmidt, R. Pettit, R. N’Guyen, A. Lehman, and K. Clay helped with spider maintenance. W. Wagner, D. Ledger, J. Stevens, and J.P. Gibert provided us feedback on this manuscript.

Author contribution statement

MCC, JPD, and EH conceived the ideas and designed methodology, MCC collected and analyzed the data, MCC wrote the first version of the manuscript, and all authors contributed to subsequent versions.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2019_4488_MOESM1_ESM.pdf (70 kb)
Supplementary material 1 (PDF 70 kb)

References

  1. Anderson RA, Karasov WH (1981) Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards. Oecologia 49:67–72.  https://doi.org/10.1007/BF00376899 CrossRefGoogle Scholar
  2. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Advances in ecological research. Elsevier, New York, pp 1–58Google Scholar
  3. Auer SK, Salin K, Rudolf AM et al (2015) Flexibility in metabolic rate confers a growth advantage under changing food availability. J Anim Ecol 84:1405–1411.  https://doi.org/10.1111/1365-2656.12384 CrossRefGoogle Scholar
  4. Badyaev AV (2002a) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17:369–378.  https://doi.org/10.1016/S0169-5347(02)02569-7 CrossRefGoogle Scholar
  5. Badyaev AV (2002b) Male and female growth in sexually dimorphic species: harmony, conflict, or both? Comments Theor Biol 7:11–33.  https://doi.org/10.1080/08948550212973 CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using Ime4. J Stat Soft 67(1):1–48Google Scholar
  7. Beck CA, Iverson SJ, Bowen WD, Blanchard W (2007) Sex differences in grey seal diet reflect seasonal variation in foraging behaviour and reproductive expenditure: evidence from quantitative fatty acid signature analysis. J Anim Ecol 76:490–502.  https://doi.org/10.1111/j.1365-2656.2007.01215.x CrossRefGoogle Scholar
  8. Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407CrossRefGoogle Scholar
  9. Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016.  https://doi.org/10.1111/j.1439-0310.2005.01147.x CrossRefGoogle Scholar
  10. Blanckenhorn WU, Viele SNT (1999) Foraging in yellow dung flies: testing for a small-male time budget advantage. Ecol Entomol 24:1–6.  https://doi.org/10.1046/j.1365-2311.1999.00171.x CrossRefGoogle Scholar
  11. Blanckenhorn WU, Preziosi RF, Fairbairn DJ (1995) Time and energy constraints and the evolution of sexual size dimorphism—to eat or to mate? Evol Ecol 9:369–381.  https://doi.org/10.1007/BF01237760 CrossRefGoogle Scholar
  12. Blanckenhorn WU, Dixon AFG, Fairbairn DJ et al (2007) Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am Nat 169:245–257.  https://doi.org/10.1086/510597 CrossRefGoogle Scholar
  13. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135.  https://doi.org/10.1016/j.tree.2008.10.008 CrossRefGoogle Scholar
  14. Brose U (2010) Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct Ecol 24:28–34.  https://doi.org/10.1111/j.1365-2435.2009.01618.x CrossRefGoogle Scholar
  15. Brose U, Jonsson T, Berlow EL et al (2006) Consumer–resource body-size relationships in natural food webs. Ecology 87:2411–2417CrossRefGoogle Scholar
  16. Budrienė A, Budrys E, Nevronytė Ž (2013) Sexual size dimorphism in the ontogeny of the solitary predatory wasp Symmorphus allobrogus (Hymenoptera: Vespidae). C R Biol 336:57–64.  https://doi.org/10.1016/j.crvi.2013.03.001 CrossRefGoogle Scholar
  17. Carbone C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biol 5:e22.  https://doi.org/10.1371/journal.pbio.0050022 CrossRefGoogle Scholar
  18. Chelini M-C, Hebets EA (2016) Absence of mate choice and postcopulatory benefits in a species with extreme sexual size dimorphism. Ethology 122:95–104.  https://doi.org/10.1111/eth.12449 CrossRefGoogle Scholar
  19. Chelini M-C, Hebets E (2017) Field evidence challenges the often-presumed relationship between early male maturation and female-biased sexual size dimorphism. Ecol Evol 7:9592–9601CrossRefGoogle Scholar
  20. Chou C-C, Iwasa Y, Nakazawa T (2016) Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism. Evolution 70:369–384.  https://doi.org/10.1111/evo.12857 CrossRefGoogle Scholar
  21. Cox RM, Calsbeek R (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173:176–187.  https://doi.org/10.1086/595841 CrossRefGoogle Scholar
  22. Cox RM, Skelly SL, Leo A, John-Alder HB (2005) Testosterone regulates sexually dimorphic coloration in the Eastern Fence Lizard, Sceloporus undulatus. Copeia 2005:597–608.  https://doi.org/10.1643/CP-04-313R CrossRefGoogle Scholar
  23. DeLong JP (2012) Experimental demonstration of a ‘rate–size’ trade-off governing body size optimization. Evol Ecol Res 14:343–352Google Scholar
  24. DeLong JP, Gilbert B, Shurin JB et al (2015) The body size dependence of trophic cascades. Am Nat 185:354–366.  https://doi.org/10.1086/679735 CrossRefGoogle Scholar
  25. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116.  https://doi.org/10.1111/j.1469-185X.2010.00136.x CrossRefGoogle Scholar
  26. Dodson GN, Beck MW (1993) Pre-copulatory guarding of penultimate females by male crab spiders, Misumenoides formosipes. Anim Behav 46:951–959.  https://doi.org/10.1006/anbe.1993.1276 CrossRefGoogle Scholar
  27. Dodson GN, Anderson AG, Stellwag LM (2015) Movement, sex ratio, and population density in a dwarf male spider species, Misumenoides formosipes (Araneae: Thomisidae). J Arachnol 43:388–393.  https://doi.org/10.1636/arac-43-03-388-393 CrossRefGoogle Scholar
  28. Downs CJ, Brown JL, Wone BWM et al (2016) Speeding up growth: selection for mass-independent maximal metabolic rate alters growth rates. Am Nat 187:295–307.  https://doi.org/10.1086/684837 CrossRefGoogle Scholar
  29. Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu Rev Ecol Syst 2:659–687CrossRefGoogle Scholar
  30. Foelix RF (2011) Biology of spiders, 3rd edn. Oxford University Press, Oxford, New YorkGoogle Scholar
  31. Foellmer MW, Moya-Larano J (2007) Sexual size dimorphism in spiders: patterns and processes. In: Sex, size and render roles: evolutionary studies of sexual size dimorphism. Oxford Biol , p 266Google Scholar
  32. Forster J, Hirst AG (2012) The temperature-size rule emerges from ontogenetic differences between growth and development rates: Ontogenetic differences between growth and development rates. Funct Ecol 26:483–492.  https://doi.org/10.1111/j.1365-2435.2011.01958.x CrossRefGoogle Scholar
  33. Fuselier L, Decker P, Lunski J et al (2007) Sex differences and size at emergence are not linked to biased sex ratios in the Common Green Darner, Anax junius (Odonata: Aeshnidae). J Freshw Ecol 22:107–117.  https://doi.org/10.1080/02705060.2007.9664151 CrossRefGoogle Scholar
  34. Gade G (2002) Sexual dimorphism in the pyrgomorphid grasshopper Phymateus morbillosus: from wing morphometry and flight behaviour to flight physiology and endocrinology. Physiol Entomol 27:51–57.  https://doi.org/10.1046/j.1365-3032.2002.00268.x CrossRefGoogle Scholar
  35. Garel M, Solberg EJ, Sæther B-E et al (2006) The length of growing season and adult sex ratio affect sexual size dimorphism in moose. Ecology 87:745–758CrossRefGoogle Scholar
  36. Gillooly JF, Brown JH, West GB et al (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251.  https://doi.org/10.1126/science.1061967 CrossRefGoogle Scholar
  37. Gillooly JF, Allen AP, West GB, Brown JH (2005) The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc Natl Acad Sci 102:140–145.  https://doi.org/10.1073/pnas.0407735101 CrossRefGoogle Scholar
  38. González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390–398.  https://doi.org/10.1034/j.1600-0706.2000.900220.x CrossRefGoogle Scholar
  39. Hirst AG, Horne CR, Atkinson D (2015) Equal temperature–size responses of the sexes are widespread within arthropod species. Proc R Soc B Biol Sci 282:20152475.  https://doi.org/10.1098/rspb.2015.2475 CrossRefGoogle Scholar
  40. Holtby LB, Healey MC (1990) Sex-specific life history tactics and risk-taking in Coho Salmon. Ecology 71:678–690.  https://doi.org/10.2307/1940322 CrossRefGoogle Scholar
  41. Honěk A, Honek A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483.  https://doi.org/10.2307/3544943 CrossRefGoogle Scholar
  42. Hormiga G, Scharff N, Coddington JA (2000) The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Syst Biol 49:435–462.  https://doi.org/10.1080/10635159950127330 CrossRefGoogle Scholar
  43. Hou C, Zuo W, Moses ME et al (2008) Energy uptake and allocation during ontogeny. Science 322:736–739.  https://doi.org/10.1126/science.1162302 CrossRefGoogle Scholar
  44. Isaac JL (2005) Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Rev 35:101–115.  https://doi.org/10.1111/j.1365-2907.2005.00045.x CrossRefGoogle Scholar
  45. Legrand RS, Morse DH (2000) Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density. Biol J Linn Soc 71:643–664.  https://doi.org/10.1111/j.1095-8312.2000.tb01283.x CrossRefGoogle Scholar
  46. Leigh SR, Shea BT (1996) Ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43–65.  https://doi.org/10.1002/(SICI)1096-8644(199601)99:1%3c43:AID-AJPA3%3e3.0.CO;2-0 CrossRefGoogle Scholar
  47. Mikolajewski DJ, Brodin T, Johansson F, Joop G (2005) Phenotypic plasticity in gender specific life-history: effects of food availability and predation. Oikos 110:91–100.  https://doi.org/10.1111/j.0030-1299.2005.13766.x CrossRefGoogle Scholar
  48. Morse DH (2013) Reproductive output of a female crab spider: the impacts of mating failure, natural enemies, and resource availability. Entomol Exp Appl 146:141–148.  https://doi.org/10.1111/j.1570-7458.2012.01301.x CrossRefGoogle Scholar
  49. Moses ME, Hou C, Woodruff WH et al (2008) Revisiting a model of ontogenetic growth: estimating model parameters from theory and data. Am Nat 171:632–645.  https://doi.org/10.1086/587073 CrossRefGoogle Scholar
  50. Muniappan R, Chada HL (1970) Biology of the crab spider, Misumenops celer. Ann Entomol Soc Am 63:1718–1722.  https://doi.org/10.1093/aesa/63.6.1718 CrossRefGoogle Scholar
  51. Norberg RA (1977) An ecological theory on foraging time and energetics and choice of optimal food-searching method. J Anim Ecol 46:511.  https://doi.org/10.2307/3827 CrossRefGoogle Scholar
  52. O’Mara MT, Gordon AD, Catlett KK et al (2012) Growth and the development of sexual size dimorphism in lorises and galagos. Am J Phys Anthropol 147:11–20.  https://doi.org/10.1002/ajpa.21600 CrossRefGoogle Scholar
  53. Ono KA, Boness DJ (1996) Sexual dimorphism in sea lion pups: differential maternal investment, or sex-specific differences in energy allocation? Behav Ecol Sociobiol 38:31–41CrossRefGoogle Scholar
  54. Prenter J, Montgomery WI, Elwood RW (1995) Multivariate morphometrics and sexual dimorphism in the orb-web spider Metellina segmentata (Clerck, 1757) (Araneae, Metidae). Biol J Linn Soc 55:345–354.  https://doi.org/10.1111/j.1095-8312.1995.tb01070.x CrossRefGoogle Scholar
  55. Preziosi RF, Fairbairn DJ (2000) Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism. Evolution 54:558–566.  https://doi.org/10.1111/j.0014-3820.2000.tb00058.x CrossRefGoogle Scholar
  56. Preziosi RF, Fairbairn DJ, Roff DA, Brennan JM (1996) Body size and fecundity in the waterstrider Aquarius remigis: a test of Darwin’s fecundity advantage hypothesis. Oecologia 108:424–431CrossRefGoogle Scholar
  57. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  58. Rennie MD, Purchase CF, Lester N et al (2008) Lazy males? Bioenergetic differences in energy acquisition and metabolism help to explain sexual size dimorphism in percids. J Anim Ecol 77:916–926.  https://doi.org/10.1111/j.1365-2656.2008.01412.x CrossRefGoogle Scholar
  59. Ricklefs RE (2003) Is rate of ontogenetic growth constrained by resource supply or tissue growth potential? A comment on West et al’s model. Funct Ecol 17:384–393.  https://doi.org/10.1046/j.1365-2435.2003.00745.x CrossRefGoogle Scholar
  60. Riede JO, Brose U, Ebenman B et al (2011) Stepping in Elton’s footprints: a general scaling model for body masses and trophic levels across ecosystems: stepping in Elton’s footprints. Ecol Lett 14:169–178.  https://doi.org/10.1111/j.1461-0248.2010.01568.x CrossRefGoogle Scholar
  61. Rohner PT, Blanckenhorn WU, Schäfer MA (2017) Critical weight mediates sex-specific body size plasticity and sexual dimorphism in the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae). Evol Dev 19:147–156.  https://doi.org/10.1111/ede.12223 CrossRefGoogle Scholar
  62. Rohner PT, Teder T, Esperk T et al (2018) The evolution of male-biased sexual size dimorphism is associated with increased body size plasticity in males. Funct Ecol 32:581–591.  https://doi.org/10.1111/1365-2435.13004 CrossRefGoogle Scholar
  63. Savage VM, Gillooly JF, Brown JH et al (2004) Effects of body size and temperature on population growth. Am Nat 163:429–441.  https://doi.org/10.1086/381872 CrossRefGoogle Scholar
  64. Scharff N, Coddington JA (1997) A phylogenetic analysis of the orb-weaving spider family Araneidae (Arachnida, Araneae). Zool J Linn Soc 120:355–434.  https://doi.org/10.1111/j.1096-3642.1997.tb01281.x CrossRefGoogle Scholar
  65. Schmalhofer VR (2011) Impacts of temperature, hunger and reproductive condition on metabolic rates of flower-dwelling crab spiders (Araneae: Thomisidae). J Arachnol 39:41–52.  https://doi.org/10.1636/Hi09-103.1 CrossRefGoogle Scholar
  66. Shillington C, Peterson CC (2002) Energetics of male and female tarantulas. J Exp Biol 205:2909–2914Google Scholar
  67. Shine Richard (1988) The evolution of large body size in females: a critique of Darwin’s “Fecundity Advantage” model. Am Nat 131:124–131CrossRefGoogle Scholar
  68. Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–461CrossRefGoogle Scholar
  69. Shine R (1994) Sexual size dimorphism in snakes revisited. Copeia 1994:326.  https://doi.org/10.2307/1446982 CrossRefGoogle Scholar
  70. Smith RJ, Leigh SR (1998) Sexual dimorphism in primate neonatal body mass. J Hum Evol 34:173–201.  https://doi.org/10.1006/jhev.1997.0190 CrossRefGoogle Scholar
  71. Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51:3–47.  https://doi.org/10.1086/409052 CrossRefGoogle Scholar
  72. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259.  https://doi.org/10.2307/2389364 CrossRefGoogle Scholar
  73. Stillwell RC, Davidowitz G (2010) Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual size dimorphism. Proc R Soc B Biol Sci 277:3819–3826.  https://doi.org/10.1098/rspb.2010.0895 CrossRefGoogle Scholar
  74. Stillwell RC, Blanckenhorn WU, Teder T et al (2010) Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu Rev Entomol 55:227–245.  https://doi.org/10.1146/annurev-ento-112408-085500 CrossRefGoogle Scholar
  75. Tammaru T, Esperk T (2007) Growth allometry of immature insects: larvae do not grow exponentially. Funct Ecol 21:1099–1105.  https://doi.org/10.1111/j.1365-2435.2007.01319.x CrossRefGoogle Scholar
  76. Tammaru T, Esperk T, Ivanov V, Teder T (2010) Proximate sources of sexual size dimorphism in insects: locating constraints on larval growth schedules. Evol Ecol 24:161–175.  https://doi.org/10.1007/s10682-009-9297-1 CrossRefGoogle Scholar
  77. Teder T (2014) Sexual size dimorphism requires a corresponding sex difference in development time: a meta-analysis in insects. Funct Ecol 28:479–486.  https://doi.org/10.1111/1365-2435.12172 CrossRefGoogle Scholar
  78. Teder T, Tammaru T (2005) Sexual size dimorphism within species increases with body size in insects. Oikos 108:321–334.  https://doi.org/10.1111/j.0030-1299.2005.13609.x CrossRefGoogle Scholar
  79. Tenhumberg B, Tyre AJ, Roitberg B (2000) Stochastic variation in food availability influences weight and age at maturity. J Theor Biol 202:257–272.  https://doi.org/10.1006/jtbi.1999.1049 CrossRefGoogle Scholar
  80. Trabalon M, Blais C (2012) Juvenile development, ecdysteroids and hemolymph level of metabolites in the spider Brachypelma albopilosum (Theraphosidae). J Exp Zool Part Ecol Genet Physiol 317:236–247.  https://doi.org/10.1002/jez.1717 CrossRefGoogle Scholar
  81. Vendl T, Kratochvíl L, Šípek P (2016) Ontogeny of sexual size dimorphism in the hornless rose chafer Pachnoda marginata (Coleoptera: Scarabaeidae: Cetoniinae). Zoology 119:481–488.  https://doi.org/10.1016/j.zool.2016.07.002 CrossRefGoogle Scholar
  82. Vendl T, Šípek P, Kouklík O, Kratochvíl L (2018) Hidden complexity in the ontogeny of sexual size dimorphism in male-larger beetles. Sci Rep 8:5871.  https://doi.org/10.1038/s41598-018-24047-1 CrossRefGoogle Scholar
  83. Vollrath F (1998) Dwarf males. Trends Ecol Evol 13:159–163.  https://doi.org/10.1016/S0169-5347(97)01283-4 CrossRefGoogle Scholar
  84. Vollrath F, Parker GA (1992) Sexual dimorphism and distorted sex ratios in spiders. Nature 360:156–159.  https://doi.org/10.1038/360156a0 CrossRefGoogle Scholar
  85. Walker SE, Rypstra AL (2001) Sexual dimorphism in functional response and trophic morphology in Rabidosa rabida (Araneae: Lycosidae). Am Midl Nat 146:161–170.  https://doi.org/10.1674/0003-0031(2001)146%5b0161:sdifra%5d2.0.co;2 CrossRefGoogle Scholar
  86. Walker SE, Rypstra AL (2002) Sexual dimorphism in trophic morphology and feeding behavior of wolf spiders (Araneae: Lycosidae) as a result of differences in reproductive roles. Can J Zool 80:679–688.  https://doi.org/10.1139/z02-037 CrossRefGoogle Scholar
  87. Weatherhead PJ, Teather KL (1994) Sexual size dimorphism and egg-size allometry in birds. Evolution 48:671–678.  https://doi.org/10.1111/j.1558-5646.1994.tb01352.x CrossRefGoogle Scholar
  88. West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631.  https://doi.org/10.1038/35098076 CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Natural SciencesUniversity of California, MercedMercedUSA
  2. 2.School of Biological SciencesUniversity of Nebraska-LincolnLincolnUSA

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