1932

Abstract

Sexual size dimorphism is one of the most striking animal traits, and among terrestrial animals, it is most extreme in certain spider lineages. The most extreme sexual size dimorphism (eSSD) is female biased. eSSD itself is probably an epiphenomenon of gendered evolutionary drivers whose strengths and directions are diverse. We demonstrate that eSSD spider clades are aberrant by sampling randomly across all spiders to establish overall averages for female (6.9 mm) and male (5.6 mm) size. At least 16 spider eSSD clades exist. We explore why the literature does not converge on an overall explanation for eSSD and propose an equilibrium model featuring clade- and context-specific drivers of gender size variation. eSSD affects other traits such as sexual cannibalism, genital damage, emasculation, and monogyny with terminal investment. Coevolution with these extreme sexual phenotypes is termed eSSD mating syndrome. Finally, as costs of female gigantism increase with size, eSSD may represent an evolutionary dead end.

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2020-01-07
2024-04-18
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Literature Cited

  1. 1. 
    Agnarsson I. 2002. Sharing a web: on the relation of sociality and kleptoparasitism in theridiid spiders (Theridiidae, Araneae). J. Arachnol. 30:2181–88
    [Google Scholar]
  2. 2. 
    Agnarsson I. 2011. Habitat patch size and isolation as predictors of occupancy and number of argyrodine spider kleptoparasites in Nephila webs. Naturwissenschaften 98:2163–67
    [Google Scholar]
  3. 3. 
    Agnarsson I, Avilés L, Coddington JA, Maddison WP 2006. Sociality in theridiid spiders: repeated origins of an evolutionary dead end. Evolution 60:112342–51
    [Google Scholar]
  4. 4. 
    Andersson M, Simmons LW. 2006. Sexual selection and mate choice. Trends Ecol. Evol. 21:6296–302
    [Google Scholar]
  5. 5. 
    Andrade MCB. 1996. Sexual selection for male sacrifice in the Australian redback spider. Science 271:524570–72
    [Google Scholar]
  6. 6. 
    Andrade MCB. 2003. Risky mate search and male self-sacrifice in redback spiders. Behav. Ecol. 14:4531–38
    [Google Scholar]
  7. 7. 
    Andrade MCB, Kasumovic MM. 2005. Terminal investment strategies and male mate choice: extreme tests of Bateman. Integr. Comp. Biol. 45:5838–47
    [Google Scholar]
  8. 8. 
    Arnqvist G. 1992. Courtship behavior and sexual cannibalism in the semi-aquatic fishing spider, Dolomedesfimbriatus (Clerk) (Araneae:Pisauridae). J. Arachnol. 20:222–26
    [Google Scholar]
  9. 9. 
    Beier M. 1934. Mantodea, Fam. Mantidae, Subfam. Sibyllinae, Empusinae Brussels: Verteneuil & Desmet
  10. 10. 
    Biaggio MD, Sandomirsky I, Lubin Y, Harari AR, Andrade MCB 2016. Copulation with immature females increases male fitness in cannibalistic widow spiders. Biol. Lett. 12:20160516
    [Google Scholar]
  11. 11. 
    Bilde T, Maklakov AA, Schilling N 2007. Inbreeding avoidance in spiders: evidence for rescue effect in fecundity of female spiders with outbreeding opportunity. J. Evol. Biol. 20:31237–42
    [Google Scholar]
  12. 12. 
    Blackledge TA, Kuntner M, Agnarsson I 2011. The form and function of spider orb webs: evolution from silk to ecosystems. Adv. Insect Phys. 41:175–262
    [Google Scholar]
  13. 13. 
    Blamires SJ, Hochuli DF, Thompson MB 2009. Prey protein influences growth and decoration building in the orb web spider Argiopekeyserlingi. Ecol. Entomol 34:5545–50
    [Google Scholar]
  14. 14. 
    Blanckenhorn WU. 2005. Behavioral causes and consequences of sexual size dimorphism. Ethology 111:11977–1016
    [Google Scholar]
  15. 15. 
    Blanckenhorn WU, Dixon AFG, Fairbairn DJ, Foellmer MW, Gibert P et al. 2007. Proximate causes of Rensch's Rule: Does sexual size dimorphism in arthropods result from sex differences in development time?. Am. Nat. 169:2245–57
    [Google Scholar]
  16. 16. 
    Blanckenhorn WU, Meier R, Teder T 2007. Rensch's rule in insects: patterns among and within species. See Ref. 39 60–70
  17. 17. 
    Blanckenhorn WU, Stillwell RC, Young KA, Fox CW, Ashton KG 2006. When Rensch meets Bergmann: Does sexual size dimorphism change systematically with latitude?. Evolution 60:102004–11
    [Google Scholar]
  18. 18. 
    Brandt Y, Andrade MCB. 2007. Testing the gravity hypothesis of sexual size dimorphism: Are small males faster climbers?. Funct. Ecol. 21:2379–85
    [Google Scholar]
  19. 19. 
    Brockhurst MA, Chapman T, King KC, Mank JE, Paterson S, Hurst GDD 2014. Running with the Red Queen: the role of biotic conflicts in evolution. Proc. R. Soc. B 281:179720141382
    [Google Scholar]
  20. 20. 
    Ceballos Meraz L, Henaut Y, Elgar MA 2012. Effects of male size and female dispersion on male mate-locating success in Nephilaclavipes. J. Ethol 30:193–100
    [Google Scholar]
  21. 21. 
    Chelini MC, Hebets EA. 2016. Absence of mate choice and postcopulatory benefits in a species with extreme sexual size dimorphism. Ethology 122:295–104
    [Google Scholar]
  22. 22. 
    Cheng R-C. 2015. Evolutionary patterns and processes resulting in extreme sexual dimorphism in the spider group Argiopinae PhD Diss., Univ. Ljubljana, Slov.
  23. 23. 
    Cheng R-C, Kuntner M. 2014. Phylogeny suggests non-directional and isometric evolution of sexual size dimorphism in argiopine spiders. Evolution 68:102861–72
    [Google Scholar]
  24. 24. 
    Cheng R-C, Kuntner M. 2015. Disentangling the size and shape components of sexual dimorphism. Evol. Biol. 42:2223–34
    [Google Scholar]
  25. 25. 
    Cheng R-C, Yang E-C, Lin C-P, Herberstein ME, Tso I-M 2010. Insect form vision as one potential shaping force of spider web decoration design. J. Exp. Biol. 213:759–68
    [Google Scholar]
  26. 26. 
    Coddington JA, Hormiga G, Scharff N 1997. Giant female or dwarf male spiders?. Nature 385:687–88
    [Google Scholar]
  27. 27. 
    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
    [Google Scholar]
  28. 28. 
    Cox RM, Butler MA, John-Alder HB 2007. The evolution of sexual size dimorphism in reptiles. See Ref. 39 38–49
  29. 29. 
    Cox RM, Calsbeek R. 2009. Sex-specific selection and intraspecific variation in sexual size dimorphism. Evolution 64:3798–809
    [Google Scholar]
  30. 30. 
    Danielson-François A, Hou C, Cole N, Tso IM 2012. Scramble competition for moulting females as a driving force for extreme male dwarfism in spiders. Anim. Behav. 84:4937–45
    [Google Scholar]
  31. 31. 
    Depa Ł, Kanturski M, Junkiert Ł, Wieczorek K 2015. Giant females versus dwarfish males of the genus Stomaphis Walker (Hemiptera: Aphididae): an aphid example of the ongoing course to permanent parthenogenesis?. Arthropod Syst. Phylogeny 73:119–40
    [Google Scholar]
  32. 32. 
    Eberhard WG. 2004. Why study spider sex: Special traits of spiders facilitate studies of sperm competition and cryptic female choice. J. Arachnol. 32:3545–56
    [Google Scholar]
  33. 33. 
    Elgar MA. 1991. Sexual cannibalism, size dimorphism, and courtship in orb-weaving spiders (Araneidae). Evolution 45:2444–48
    [Google Scholar]
  34. 34. 
    Elgar MA. 1993. Inter-specific associations involving spiders: kleptoparasitism, mimicry, and mutualism. Mem. Queensl. Museum 33:June411–30
    [Google Scholar]
  35. 35. 
    Elgar MA, De Crespigny FEC, Ramamurthy S 2003. Male copulation behaviour and the risk of sperm competition. Anim. Behav. 66:211–16
    [Google Scholar]
  36. 36. 
    Elgar MA, Schneider JM. 2004. Evolutionary significance of sexual cannibalism. Adv. Study Behav. 34:135–63
    [Google Scholar]
  37. 37. 
    Esperk T, Tammaru T, Nylin S, Teder T 2007. Achieving high sexual size dimorphism in insects: Females add instars. Ecol. Entomol. 32:3243–56
    [Google Scholar]
  38. 38. 
    Fairbairn DJ. 2007. Introduction: the enigma of sexual size dimorphism. See Ref. 39 1–10
  39. 39. 
    Fairbarn DJ, Blanckenhorn WU, Székely T, eds. 2007. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  40. 40. 
    Foellmer MW. 2008. Broken genitals function as mating plugs and affect sex ratios in the orb-web spider Argiopeaurantia. Evol. Ecol. Res 10:3449–62
    [Google Scholar]
  41. 41. 
    Foellmer MW, Fairbairn DJ. 2003. Spontaneous male death during copulation in an orb-weaving spider. Proc. R. Soc. B 270:S183–85
    [Google Scholar]
  42. 42. 
    Foellmer MW, Fairbairn DJ. 2005. Competing dwarf males: sexual selection in an orb-weaving spider. J. Evol. Biol. 18:3629–41
    [Google Scholar]
  43. 43. 
    Foellmer MW, Moya-Laraño J. 2007. Sexual size dimorphism in spiders: patterns and processes. See Ref. 39 71–82
  44. 44. 
    Fox LR. 1975. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6:87–106
    [Google Scholar]
  45. 45. 
    Fromhage L, Jacobs K, Schneider JM 2007. Monogynous mating behaviour and its ecological basis in the golden orb spider Nephilafenestrata. Ethology 113:8813–20
    [Google Scholar]
  46. 46. 
    Fromhage L, McNamara JM, Houston AI 2008. A model for the evolutionary maintenance of monogyny in spiders. J. Theor. Biol. 250:3524–31
    [Google Scholar]
  47. 47. 
    Fromhage L, Schneider JM. 2005. Safer sex with feeding females: sexual conflict in a cannibalistic spider. Behav. Ecol. 16:2377–82
    [Google Scholar]
  48. 48. 
    Gregorič M, Agnarsson I, Blackledge TA, Kuntner M 2011. Darwin's bark spider: giant prey in giant orb webs (Caerostrisdarwini, Araneae: Araneidae)?. J. Arachnol. 39:2287–95
    [Google Scholar]
  49. 49. 
    Gregorič M, Agnarsson I, Blackledge TA, Kuntner M 2015. Phylogenetic position and composition of Zygiellinae and Caerostris, with new insight into orb-web evolution and gigantism. Zool. J. Linn. Soc. 175:2225–43
    [Google Scholar]
  50. 50. 
    Gregorič M, Blackledge TA, Agnarsson I, Kuntner M 2015. A molecular phylogeny of bark spiders reveals new species from Africa and Madagascar (Araneae: Araneidae: Caerostris). J. Arachnol. 43:293–312
    [Google Scholar]
  51. 51. 
    Gregorič M, Šuen K, Cheng R-C, Kralj-Fišer S, Kuntner M 2016. Spider behaviors include oral sexual encounters. Sci. Rep. 6:April25128
    [Google Scholar]
  52. 52. 
    Gröning J, Hochkirch A. 2008. Reproductive interference between animal species. Q. Rev. Biol. 83:3257–82
    [Google Scholar]
  53. 53. 
    Grossi B, Canals M. 2015. Energetics, scaling and sexual size dimorphism of spiders. Acta Biotheor 63:171–81
    [Google Scholar]
  54. 54. 
    Head G. 1995. Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (Class Araneae). Evolution 49:4776–81
    [Google Scholar]
  55. 55. 
    Herberstein ME, Painting CJ, Holwell GI 2017. Scramble competition polygyny in terrestrial arthropods. Adv. Stud. Behav. 49:237–95
    [Google Scholar]
  56. 56. 
    Higgins L. 1993. Constraints and plasticity in the development of juvenile Nephilaclavipes in Mexico. J. Arachnol. 21:2107–19
    [Google Scholar]
  57. 57. 
    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. 25:61289–306
    [Google Scholar]
  58. 58. 
    Higgins LE. 1992. Developmental plasticity and fecundity in the orb-weaving spider Nephilaclavipes. J. Arachnol 20:294–106
    [Google Scholar]
  59. 59. 
    Holdsworth AR, Morse DH. 2000. Mate guarding and aggression by the crab spider Misumenavatia in relation to female reproductive status and sex ratio. Am. Midl. Nat. 143:1201–11
    [Google Scholar]
  60. 60. 
    Hormiga G, Scharff N, Coddington JA 2000. The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Syst. Biol. 49:3435–62
    [Google Scholar]
  61. 61. 
    Inkpen SA, Foellmer MW. 2010. Sex-specific foraging behaviours and growth rates in juveniles contribute to the development of extreme sexual size dimorphism in a spider. Open Ecol. J. 3:59–70
    [Google Scholar]
  62. 62. 
    Johnson JC. 2001. Sexual cannibalism in fishing spiders (Dolomedestriton): an evaluation of two explanations for female aggression towards potential mates. Anim. Behav. 61:905–14
    [Google Scholar]
  63. 63. 
    Johnson JC. 2005. The role of body size in mating interactions of the sexually cannibalistic fishing spider Dolomedestriton. Ethology 111:151–61
    [Google Scholar]
  64. 64. 
    Johnson JC, Sih A. 2005. Precopulatory sexual cannibalism in fishing spiders (Dolomedestriton): a role for behavioral syndromes. Behav. Ecol. Sociobiol. 58:4390–96
    [Google Scholar]
  65. 65. 
    Jones TM, Elgar MA. 2008. Male insemination decisions and sperm quality influence paternity in the golden orb-weaving spider. Behav. Ecol. 19:2285–91
    [Google Scholar]
  66. 66. 
    Kallal RJ, Hormiga G. 2018. Systematics, phylogeny and biogeography of the Australasian leaf-curling orb-weaving spiders (Araneae: Araneidae: Zygiellinae), with a comparative analysis of retreat evolution. Zool. J. Linn. Soc. 184:41055–141
    [Google Scholar]
  67. 67. 
    Kasumovic MM, Bruce MJ, Andrade MC, Herberstein ME 2008. Spatial and temporal demographic variation drives within-season fluctuations in sexual selection. Evolution 62:92316–25
    [Google Scholar]
  68. 68. 
    Kasumovic MM, Bruce MJ, Herberstein ME, Andrade MCB 2007. Risky mate search and mate preference in the golden orb-web spider (Nephilaplumipes). Behav. Ecol. 18:1189–95
    [Google Scholar]
  69. 69. 
    Kasumovic MM, Bruce MJ, Herberstein ME, Andrade MCB 2009. Evidence for developmental plasticity in response to demographic variation in nature. Ecology 90:82287–96
    [Google Scholar]
  70. 70. 
    Kralj-Fišer S, Čandek K, Lokovšek T, Čelik T, Cheng R-C et al. 2016. Mate choice and sexual size dimorphism, not personality, explain female aggression and sexual cannibalism in raft spiders. Anim. Behav. 111:49–55
    [Google Scholar]
  71. 71. 
    Kralj-Fišer S, Gregorič M, Zhang S, Li D, Kuntner M 2011. Eunuchs are better fighters. Anim. Behav. 81:5933–39
    [Google Scholar]
  72. 72. 
    Kralj-Fišer S, Kuntner M. 2012. Eunuchs as better fighters?. Naturwissenschaften 99:295–101
    [Google Scholar]
  73. 73. 
    Kralj-Fišer S, Schneider JM, Justinek Ž, Kalin S, Gregorič M et al. 2012. Mate quality, not aggressive spillover, explains sexual cannibalism in a size-dimorphic spider. Behav. Ecol. Sociobiol. 66:1145–51
    [Google Scholar]
  74. 74. 
    Kuntner M. 2005. A revision of Herennia (Araneae: Nephilidae: Nephilinae), the Australasian “coin spiders.”. Invertebr. Syst. 19:5391–436
    [Google Scholar]
  75. 75. 
    Kuntner M, Agnarsson I. 2010. Web gigantism in Darwin's bark spider, a new species from Madagascar (Araneidae: Caerostris). J. Arachnol. 38:346–56
    [Google Scholar]
  76. 76. 
    Kuntner M, Agnarsson I, Gregorič M 2009. Nephilid spider eunuch phenomenon induced by female or rival male aggressiveness. J. Arachnol. 37:3266–71
    [Google Scholar]
  77. 77. 
    Kuntner M, Agnarsson I, Li D 2015. The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders. Biol. Rev. 90:1279–96
    [Google Scholar]
  78. 78. 
    Kuntner M, Arnedo MA, Trontelj P, Lokovšek T, Agnarsson I 2013. A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage. Mol. Phylogenet. Evol. 69:3961–79
    [Google Scholar]
  79. 79. 
    Kuntner M, Cheng R-C. 2016. Evolutionary pathways maintaining extreme female-biased sexual size dimorphism: convergent spider cases defy common patterns. Evolutionary Biology: Convergent Evolution, Evolution of Complex Traits, Concepts and Methods P Pontarotti 121–33 Berlin: Springer
    [Google Scholar]
  80. 80. 
    Kuntner M, Cheng R-C, Kralj-Fišer S, Liao C-P, Schneider JM, Elgar MA 2016. The evolution of genital complexity and mating rates in sexually size dimorphic spiders. BMC Evol. Biol. 16:1242
    [Google Scholar]
  81. 81. 
    Kuntner M, Coddington JA. 2009. Discovery of the largest orbweaving spider species: the evolution of gigantism in Nephila. PLOS ONE 4:10e7516
    [Google Scholar]
  82. 82. 
    Kuntner M, Coddington JA, Schneider JM 2009. Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution 63:61451–63
    [Google Scholar]
  83. 83. 
    Kuntner M, Elgar MA. 2014. Evolution and maintenance of sexual size dimorphism: aligning phylogenetic and experimental evidence. Front. Ecol. Evol. 2:26
    [Google Scholar]
  84. 84. 
    Kuntner M, Gregorič M, Li D 2010. Mass predicts web asymmetry in Nephila spiders. Naturwissenschaften 97:121097–105
    [Google Scholar]
  85. 85. 
    Kuntner M, Haddad CR, Aljančič G, Blejec A 2008. Ecology and web allometry of Clitaetrairenae, an arboricolous African orb-weaving spider (Araneae, Araneoidea, Nephilidae). J. Arachnol. 36:3583–94
    [Google Scholar]
  86. 86. 
    Kuntner M, Hamilton CA, Cheng R-C, Gregorič M, Lupše N et al. 2019. Golden orbweavers ignore biological rules: phylogenomic and comparative analyses unravel a complex evolution of sexual size dimorphism. Syst. Biol. 68:4555–72
    [Google Scholar]
  87. 87. 
    Kuntner M, Kralj-Fišer S, Gregorič M 2010. Ladder webs in orb-web spiders: ontogenetic and evolutionary patterns in Nephilidae. Biol. J. Linn. Soc. 99:4849–66
    [Google Scholar]
  88. 88. 
    Kuntner M, Kralj-Fišer S, Schneider JM, Li D 2009. Mate plugging via genital mutilation in nephilid spiders: an evolutionary hypothesis. J. Zool. 277:4257–66
    [Google Scholar]
  89. 89. 
    Kuntner M, Pristovšek U, Cheng R-C, Li D, Zhang S et al. 2015. Eunuch supremacy: evolution of post-mating spider emasculation. Behav. Ecol. Sociobiol. 69:1117–26
    [Google Scholar]
  90. 90. 
    Kuntner M, Zhang S, Gregorič M, Li D 2012. Nephila female gigantism attained through post-maturity molting. J. Arachnol. 40:3345–47
    [Google Scholar]
  91. 91. 
    Kupfer A. 2007. Sexual size dimorphism in amphibians: an overview. See Ref. 39 50–59
  92. 92. 
    Lee QQ, Oh J, Kralj-Fišer S, Kuntner M, Li D 2012. Emasculation: Gloves-off strategy enhances eunuch spider endurance. Biol. Lett. 8:5733–35
    [Google Scholar]
  93. 93. 
    Legrand RS, Morse DH. 2000. Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density. Biol. J. Linn. Soc. 71:4643–64
    [Google Scholar]
  94. 94. 
    Li D, Oh J, Kralj-Fišer S, Kuntner M 2012. Remote copulation: male adaptation to female cannibalism. Biol. Lett. 8:4512–15
    [Google Scholar]
  95. 95. 
    Lindenfors P, Gittleman JL, Jones KE 2007. Sexual size dimorphism in mammals. See Ref. 39 16–26
  96. 96. 
    Lomolino MV. 1985. Body size of mammals on islands: the island rule reexamined. Am. Nat. 125:2310–16
    [Google Scholar]
  97. 97. 
    Lovich JE, Gibbons JW. 1992. A review of techniques for quantifying sexual size dimorphism. Growth Dev. Aging 56:4269–81
    [Google Scholar]
  98. 98. 
    Lupše N, Cheng R-C, Kuntner M 2016. Coevolution of female and male genital components to avoid genital size mismatches in sexually dimorphic spiders. BMC Evol. Biol. 16:1161
    [Google Scholar]
  99. 99. 
    Lützen J, Sakamoto H, Taguchi A, Takahashi T 2001. Reproduction, dwarf males, sperm dimorphism, and life cycle in the commensal bivalve Peregrinamorohshimai Shôji (Heterodonta). Malacologia 43:1–2313–25
    [Google Scholar]
  100. 100. 
    Magalhães ILF, Santos AJ. 2012. Phylogenetic analysis of Micrathena and Chaetacis spiders (Araneae: Araneidae) reveals multiple origins of extreme sexual size dimorphism and long abdominal spines. Zool. J. Linn. Soc. 166:114–53
    [Google Scholar]
  101. 101. 
    Maklakov AA, Lubin Y. 2004. Sexual conflict over mating in a spider: Increased fecundity does not compensate for the costs of polyandry. Evolution 58:51135–40
    [Google Scholar]
  102. 102. 
    Menin M, de Jesus Rodrigues D, Salette de Azevedo C 2005. Predation on amphibians by spiders (Arachnida, Araneae) in the Neotropical region. Phyllomedusa 4:139–47
    [Google Scholar]
  103. 103. 
    Michalik P, Rittschof CC. 2011. A comparative analysis of the morphology and evolution of permanent sperm depletion in spiders. PLOS ONE 6:1e16014
    [Google Scholar]
  104. 104. 
    Miller JA. 2007. Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation. Evolution 61:61301–15
    [Google Scholar]
  105. 105. 
    Miyashita T. 1993. Male-male competition and mating success in the orb-web spider, Nephilaclavata, with reference to temporal factors. Ecol. Res. 8:193–102
    [Google Scholar]
  106. 106. 
    Modanu M, Michalik P, Andrade MCB 2013. Mating system does not predict permanent sperm depletion in black widow spiders. Evol. Dev. 15:3205–12
    [Google Scholar]
  107. 107. 
    Moya-Laraño J, Halaj J, Wise DH 2002. Climbing to reach females: Romeo should be small. Evolution 56:2420–25
    [Google Scholar]
  108. 108. 
    Moya-Laraño J, Vinković D, Allard CM, Foellmer MW 2009. Optimal climbing speed explains the evolution of extreme sexual size dimorphism in spiders. J. Evol. Biol. 22:5954–63
    [Google Scholar]
  109. 109. 
    Neumann R, Schneider JM. 2015. Differential investment and size-related mating strategies facilitate extreme size variation in contesting male spiders. Anim. Behav. 101:107–15
    [Google Scholar]
  110. 110. 
    Newman JA, Elgar MA. 1991. Sexual cannibalism in orb-weaving spiders: an economic model. Am. Nat. 138:61372–95
    [Google Scholar]
  111. 111. 
    Nyffeler M, Knörnschild M. 2013. Bat predation by spiders. PLOS ONE 8:3e58120
    [Google Scholar]
  112. 112. 
    Nyffeler M, Pusey BJ. 2014. Fish predation by semi-aquatic spiders: a global pattern. PLOS ONE 9:6e99459
    [Google Scholar]
  113. 113. 
    Parker G. 1979. Sexual selection and sexual conflict. Sexual Selection and Reproductive Competition in Insects MS Blum, NA Blum 123–66 Amsterdam: Elsevier
    [Google Scholar]
  114. 114. 
    Pascual MS. 1997. Carriage of dwarf males by adult female puelche oysters: the role of chitons. J. Exp. Mar. Biol. Ecol. 212:2173–85
    [Google Scholar]
  115. 115. 
    Peng P, Blamires SJ, Agnarsson I, Lin H-C, Tso I-M 2013. A color-mediated mutualism between two arthropod predators. Curr. Biol. 23:2172–76
    [Google Scholar]
  116. 116. 
    Preik OA, Schneider JM, Uhl G, Michalik P 2016. Transition from monogyny to polygyny in Nephilasenegalensis (Araneae: Nephilidae) is not accompanied by increased investment in sperm. Biol. J. Linn. Soc. 119:41027–35
    [Google Scholar]
  117. 117. 
    Prenter J, Elwood RW, Montgomery WI 1998. No association between sexual size dimorphism and life histories in spiders. Proc. R. Soc. B 265:139057–62
    [Google Scholar]
  118. 118. 
    Prenter J, Elwood RW, Montgomery WI 2000. Sexual size dimorphism and reproductive investment by female spiders: a comparative analysis. Evolution 53:61987–94
    [Google Scholar]
  119. 119. 
    Prenter J, Montgomery W, Elwood RW 1997. Sexual dimorphism in northern temperate spiders: implications for the differential mortality model. J. Zool. 243:341–49
    [Google Scholar]
  120. 120. 
    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 14:5e0216036
    [Google Scholar]
  121. 121. 
    Quiñones-Lebrón SG, Kralj-Fišer S, Gregorič M, Lokovšek T, Čandek K et al. 2016. Potential costs of heterospecific sexual interactions in golden orbweb spiders (Nephila spp.). Sci. Rep. 6:36908
    [Google Scholar]
  122. 122. 
    Ramos M, Coddington JA, Christenson TE, Irschick DJ 2005. Have male and female genitalia coevolved? A phylogenetic analysis of genitalic morphology and sexual size dimorphism in web-building spiders (Araneae: Araneoidea). Evolution 59:91989–99
    [Google Scholar]
  123. 123. 
    Roggenbuck H, Pekár S, Schneider JM 2011. Sexual cannibalism in the European garden spider Araneusdiadematus: the roles of female hunger and mate size dimorphism. Anim. Behav. 81:4749–55
    [Google Scholar]
  124. 124. 
    Scharff N, Coddington JA, Blackledge TA, Agnarsson I, Framenau VW et al. 2019. Phylogeny of the orb-weaving spider family Araneidae (Araneae: Araneoidea). Cladistics In press
    [Google Scholar]
  125. 125. 
    Schneider J, Fromhage L. 2010. Monogynous mating strategies in spiders. Animal Behaviour: Evolution and Mechanisms P Kappeler 441–64 Berlin: Springer
    [Google Scholar]
  126. 126. 
    Schneider J, Uhl G, Herberstein ME 2015. Cryptic female choice within the genus Argiope: a comparative approach. Cryptic Female Choice in Arthropods AV Peretti, A Aisenberg 55–77 Berlin: Springer
    [Google Scholar]
  127. 127. 
    Schneider JM. 2014. Sexual cannibalism as a manifestation of sexual conflict. Cold Spring Harb. Perspect. Biol. 6:11a017731
    [Google Scholar]
  128. 128. 
    Schneider JM, Elgar MA. 2001. Sexual cannibalism and sperm competition in the golden orb-web spider Nephilaplumipes (Araneoidea): female and male perspectives. Behav. Ecol. 12:5547–52
    [Google Scholar]
  129. 129. 
    Schneider JM, Michalik P. 2011. One-shot genitalia are not an evolutionary dead end: regained male polygamy in a sperm limited spider species. BMC Evol. Biol. 11:1197
    [Google Scholar]
  130. 130. 
    Schütz D, Taborsky M. 2000. Giant males or dwarf females: What determines the extreme sexual size dimorphism in Lamprologuscallipterus?. J. Fish Biol. 57:51254–65
    [Google Scholar]
  131. 131. 
    Schwartz SK, Wagner WE, Hebets EA 2013. Spontaneous male death and monogyny in the dark fishing spider. Biol. Lett. 9:420130113
    [Google Scholar]
  132. 132. 
    Schwartz SK, Wagner WE, Hebets EA 2014. Obligate male death and sexual cannibalism in dark fishing spiders. Anim. Behav. 93:151–56
    [Google Scholar]
  133. 133. 
    Schwartz SK, Wagner WE, Hebets EA 2016. Males can benefit from sexual cannibalism facilitated by self-sacrifice. Curr. Biol. 26:202794–99
    [Google Scholar]
  134. 134. 
    Szekely T, Lislevand T, Figuerola J 2007. Sexual size dimorphism in birds. See Ref. 39 27–37
  135. 135. 
    Thomas RF. 1977. Systematics, distribution, and biology of cephalopods of the genus Tremoctopus (Octopoda: Tremoctopodidae). Bull. Mar. Sci. 27:3353–92
    [Google Scholar]
  136. 136. 
    Tso I-M, Severinghaus LL. 1998. Silk stealing by Argyrodeslanyuensis (Araneae: Theridiidae): a unique form of kleptoparasitism. Anim. Behav. 56:1219–25
    [Google Scholar]
  137. 137. 
    Uhl G, Nessler SH, Schneider JM 2010. Securing paternity in spiders? A review on occurrence and effects of mating plugs and male genital mutilation. Genetica 138:175–104
    [Google Scholar]
  138. 138. 
    Uhl G, Vollrath F. 2000. Extreme body size variability in the golden silk spider (Nephilaedulis) does not extend to genitalia. J. Zool. 251:7–14
    [Google Scholar]
  139. 139. 
    Uhl G, Zimmer SM, Renner D, Schneider JM 2015. Exploiting a moment of weakness: Male spiders escape sexual cannibalism by copulating with moulting females. Sci. Rep. 5:16928
    [Google Scholar]
  140. 140. 
    Van Valen L. 1973. A new evolutionary law. Evol. Theory 1:1–30
    [Google Scholar]
  141. 141. 
    Venner S, Casas J. 2005. Spider webs designed for rare but life-saving catches. Proc. R. Soc. B 272:15721587–92
    [Google Scholar]
  142. 142. 
    Vollrath F. 1998. Dwarf males. Trends Ecol. Evol. 13:4159–63
    [Google Scholar]
  143. 143. 
    Vollrath F, Parker GA. 1992. Sexual dimorphism and distorted sex ratios in spiders. Nature 360:6400156–59
    [Google Scholar]
  144. 144. 
    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. 80:4679–88
    [Google Scholar]
  145. 145. 
    Walker SE, Rypstra AL. 2003. Sexual dimorphism and the differential mortality model: Is behaviour related to survival?. Biol. J. Linn. Soc. 78:197–103
    [Google Scholar]
  146. 146. 
    Webb TJ, Freckleton RP. 2007. Only half right: Species with female-biased sexual size dimorphism consistently break Rensch's Rule. PLOS ONE 2:9e897
    [Google Scholar]
  147. 147. 
    Welke KW, Schneider JM. 2012. Sexual cannibalism benefits offspring survival. Anim. Behav. 83:1201–7
    [Google Scholar]
  148. 148. 
    Wilder SM. 2011. Spider nutrition: an integrative perspective. Adv. Insect Phys. 40:87–136
    [Google Scholar]
  149. 149. 
    Wilder SM, Rypstra AL. 2008. Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders. Am. Nat. 172:3431–40
    [Google Scholar]
  150. 150. 
    Wilder SM, Rypstra AL. 2010. Males make poor meals: a comparison of nutrient extraction during sexual cannibalism and predation. Oecologia 162:3617–25
    [Google Scholar]
  151. 151. 
    Wilder SM, Rypstra AL, Elgar MA 2009. The importance of ecological and phylogenetic conditions for the occurrence and frequency of sexual cannibalism. Annu. Rev. Ecol. Evol. Syst. 40:21–39
    [Google Scholar]
  152. 152. 
    Zhan Y, Jiang H, Wu Q, Zhang H, Bai Z et al. 2019. Comparative morphology refines the conventional model of spider reproduction. PLOS ONE 14:7e0218486
    [Google Scholar]
  153. 153. 
    Zhang S, Kuntner M, Li D 2011. Mate binding: male adaptation to sexual conflict in the golden orb-web spider (Nephilidae: Nephilapilipes). Anim. Behav. 82:61299–304
    [Google Scholar]
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