Evolutionary Ecology

, 25:1289 | Cite as

Testing ecological and developmental hypotheses of mean and variation in adult size in nephilid orb-weaving spiders

  • Linden Higgins
  • Jonathan Coddington
  • Charles Goodnight
  • Matjaž Kuntner
Original Paper

Abstract

Fecundity selection has been hypothesized to drive the evolution of female gigantism in the orb-weaving family Nephilidae. Several species of these spiders also exhibit large amounts of variation in size at maturity in one or both sexes. In this article, we attempt to detect correlations of mean and variation in adult size at a phylogenetic scale between the sexes and with latitude. We tested six predictions derived from three broad developmental, ecological, and age structure hypotheses, using independent contrasts and a recent species-level nephilid phylogeny as well as least squares and other conventional statistics: 1. In both sexes, species with larger mean size will have greater variation in size; 2. Males and females will show correlated changes in mean size and of variation in size; 3. In both sexes, mean size will be negatively correlated with the midpoint of the latitudinal range; 4. In both sexes, tropical species will be more variable; 5. In both sexes, more widespread species will be more variable; 6. Variation in male size will be positively correlated with mean female size. In no cases were male and female development correlated, suggesting that in this lineage male and female body size evolve independently. The only significant trend detected was a positive phylogenetic correlation between variation in female size and latitude, the opposite of prediction 4. Power tests showed that in all tests of the ecological hypothesis, sample sizes were more than adequate to detect significant trends, if present. Our results suggest that evolutionary trends in juvenile development among species are too weak to be detectable in such data sets.

Keywords

Female gigantism Sexual size dimorphism Nephilidae Nephila Nephilengys 

References

  1. Christenson TE, Goist KC (1979) Costs and benefits of male-male competition in the orb-weaving spider, Nephila clavipes. Behav Ecol Sociobio 5:87–92CrossRefGoogle Scholar
  2. Christenson TE, Brown SG, Wenzel PA, Hill EM, Goist KC (1985) Mating behavior of the golden-orb-weaving spider, Nephila clavipes: I. Female receptivity and male courtship. J Comp Psych 99:160–166CrossRefGoogle Scholar
  3. Coddington JA (1994) The roles of homology and convergence in studies of adaptation. In: Eggleton P, Vane-Wright RI (eds) Phylogenetics and ecology. Academic Press, London, pp 53–78Google Scholar
  4. Coddington JA, Hormiga G, Scharff N (1997) Giant female or dwarf male spiders? Nature 385:687–688CrossRefGoogle Scholar
  5. Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, LondonCrossRefGoogle Scholar
  6. Dawkins R (1980) Good strategy or evolutionarily stable strategy? In: Barlow GW, Silverberg J (eds) Sociobiology: beyond nature/nurture?. Westview Press, Boulder, pp 331–367Google Scholar
  7. Dudycha JL (2003) A multi-environment comparison of senescence between sister species of Daphnia. Oecologia 135:555–563PubMedGoogle Scholar
  8. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  9. Foellmer MW, Moya-Laraño J (2007) Sexual size dimorphism in spiders: patterns and processes. In: Fairbairn DJ, Blanckenhorn WU, Szekely T (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford, pp 71–81Google Scholar
  10. Garland T, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364CrossRefGoogle Scholar
  11. Garland T Jr, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral states. Am Zool 39:374–388Google Scholar
  12. Head G (1995) Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (Class Araneae). Evolution 49:776–781CrossRefGoogle Scholar
  13. Higgins LE (1992) Developmental plasticity and fecundity in the orb-weaving spider Nephila-clavipes. J Arachnol 20:94–106Google Scholar
  14. Higgins L (1993) Constraints and plasticity in the development of juvenile Nephila clavipes in Mexico. J Arachnol 21:107–119Google Scholar
  15. Higgins L (2000) The interaction of season length and development time alters size at maturity. Oecologia 122:51–59CrossRefGoogle Scholar
  16. Higgins L (2002) Female gigantism in a New Guinea population of the spider Nephila maculata. Oikos 99:377–385CrossRefGoogle Scholar
  17. Higgins L, Goodnight C (2010) Nephila clavipes females have accelerating dietary requirements. J Arachnol 38:150–152CrossRefGoogle Scholar
  18. Higgins LE, Rankin MA (1996) Different pathways in arthropod postembryonic development. Evolution 50:573–582CrossRefGoogle Scholar
  19. Higgins LE, Rankin MA (2001) Mortality risk of rapid growth in the spider Nephila clavipes. Func Ecol 15:24–28CrossRefGoogle Scholar
  20. Hormiga G, Scharff N, Coddington JA (2000) The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Sys Bio 49:435–462CrossRefGoogle Scholar
  21. Kuntner M (2005a) Systematics and evolution of nephilid spiders (Araneae, Nephilidae new rank). George Washington University, Washington, DCGoogle Scholar
  22. Kuntner M (2005b) A revision of Herennia (Araneae, Nephilidae, Nephilinae), the Australasian “coin spiders”. Invert Syst 19:391–436CrossRefGoogle Scholar
  23. Kuntner M (2006) Phylogenetic systematics of the Gondwanan nephilid spider lineage Clitaetrinae (Araneae, Nephilidae). Zool Scr 35:19–62CrossRefGoogle Scholar
  24. Kuntner M (2007) A monograph of Nephilengys, the pantropical ‘‘hermit spiders’’ (Araneae, Nephilidae, Nephilinae). Syst Entomol 32:95–135CrossRefGoogle Scholar
  25. Kuntner M, Coddington JA (2009) Discovery of the largest orbweaving spider species: the evolution of gigantism in Nephila. PLoS ONE 4(10):7516. doi:10.1371/journal.pone.0007516 CrossRefGoogle Scholar
  26. Kuntner M, Coddington JA, Hormiga G (2008) Phylogeny of extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing morphological and ethological homologies. Cladistics 24:147–217CrossRefGoogle Scholar
  27. Kuntner M, Coddington JA, Schneider JM (2009) Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution 63:1451–1463PubMedCrossRefGoogle Scholar
  28. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–307CrossRefGoogle Scholar
  29. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.6. http://mesquiteproject.org
  30. Midford PE, Garland Jr T, Maddison WP (2007) PDAP: PDTREE Package of Mesquite, Version 1.11. http://mesquiteproject.org/pdap_mesquite/
  31. Miyashita T (1986) Growth, egg-production, and population-density of the spider, Nephila clavata in relation to food conditions in the field. Res Pop Ecol 28:135–149CrossRefGoogle Scholar
  32. Miyashita T (1991) Direct evidence of food limitation for growth rate and body size in the spider Nephila clavata. Acta Arachnol 40:17–21CrossRefGoogle Scholar
  33. Mousseau TA, Roff DA (1989) Adaptation to seasonality in a cricket: patterns of phenotypic and genotypic variation in body size and diapause expression along a cline in season length. Evolution 43:1483–1496CrossRefGoogle Scholar
  34. Nylin S, Gotthard K (1998) Plasticity in the life-history traits. Ann Rev Entom 43:63–83PubMedCrossRefGoogle Scholar
  35. Nylin S, Gotthard K, Wiklud C (1996) Reaction norms for age and size at maturity in Lasiommata butterflies: predictions and tests. Evolution 50:1351–1358CrossRefGoogle Scholar
  36. Pigliucci M, Cammell K, Schmitt J (1999) Evolution of phenotypic plasticity a comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana. J Evol Biol 12:779–791CrossRefGoogle Scholar
  37. Pollard H, Cruzan M, Pigliucci M (2001) Comparative studies of reaction norms in Arabidopsis. I. Evolution of response to daylength. Evol Ecol Res 3:129–155Google Scholar
  38. Richter-Boix A, Llorente GA, Montori A (2006) A comparative analysis of the adaptive developmental plasticity hypothesis in six mediterranean anuran species along a pond permanency gradient. Evol Ecol Res 8:1139–1154Google Scholar
  39. Robinson MH, Robinson B (1973) Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithson Contrib Zool 149:1–73CrossRefGoogle Scholar
  40. Roff DA (1980) Optimizing development time in a seasonal environment: the ‘ups and downs’ of clinal variation. Oecologia 45:202–208CrossRefGoogle Scholar
  41. Roff DA (1983) Phenological adaptation in a seasonal environment: a theoretical perspective. In: Brown VK, Hodek I (eds) Diapause and life cycle strategies in insects. Springer, New York, pp 253–270Google Scholar
  42. Roff DA (2002) Life history evolution. Sinauer Associates, MassachusettsGoogle Scholar
  43. Schneider JM (1997) Timing of maturation and the mating system of the spider, Stegodyphus lineatus (Eresidae): how important is body size? Biol J Linn Soc 60:517–525Google Scholar
  44. Schneider JM, Elgar MA (2005) The combined effects of pre- and post-insemination sexual selection on extreme variation in male body size. Evol Ecol 19:419–433CrossRefGoogle Scholar
  45. Schoener TW, Janzen DH (1968) Notes on environmental determinants of tropical versus temperate insect size patterns. Am Nat 102:207–224CrossRefGoogle Scholar
  46. Slatkin M (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630CrossRefGoogle Scholar
  47. Snedecor GW, Cochran WG (1989) Statistical methods. Blackwell Publishing, OxfordGoogle Scholar
  48. Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343Google Scholar
  49. Sultan SE, Wilczek AM, Hann SD, Brosi BJ (1998) Contrasting ecological breadth of co-occurring annual Polygonum species. J Ecol 86:363–383CrossRefGoogle Scholar
  50. Toft S (1976) Life-histories of spiders in a Danish beech wood. Nat Jutlandica 19:5–40Google Scholar
  51. Toft S (1983) Life cycles of Meta segmentata (Clerck 1757) and Meta mengei (Blackwall 1869) in western Europe (Arachnida: Araneae: Tetragnathidae). Verhandlungendes Naturwissenschaftlichen Vereins in Hamburg 26:265–276Google Scholar
  52. Uhl G, Vollrath F (2000) Extreme body size variability in the golden silk spider (Nephila edulis) does not extend to genitalia. J Zool 251:7–14CrossRefGoogle Scholar
  53. Van Buskirk J (2001) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102CrossRefGoogle Scholar
  54. Vollrath F (1980a) Why are some spider males small? A discussion on Nephila clavipes. In: Gruber J (ed) Verhandlungen. 8. Internationaler Arachnologen—Kongress abgehalten ander Universitat fur Bodenkultur Wien. H. Egermann, Vienna, pp 165–169Google Scholar
  55. Vollrath F (1980b) Male body size and fitness in the web-building spider Nephila clavipes. Z Tierpsychol 53:61–78Google Scholar
  56. Vollrath F (1998) Dwarf males. TREE 13:159–163PubMedGoogle Scholar
  57. Vollrath F, Parker GA (1992) Sexual dimorphism and distorted sex ratios in spiders. Nature 360:156–159CrossRefGoogle Scholar
  58. Vollrath F, Parker GA (1997) Reply to ‘Giant female or dwarf male spiders?’. Nature 385:688CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Linden Higgins
    • 1
  • Jonathan Coddington
    • 2
  • Charles Goodnight
    • 1
  • Matjaž Kuntner
    • 3
  1. 1.Department of BiologyUniversity of VermontBurlingtonUSA
  2. 2.National Museum of Natural History, Smithsonian InstitutionWashingtonUSA
  3. 3.Scientific Research Centre of the Slovenian Academy of Sciences and ArtsLjubljanaSlovenia

Personalised recommendations