Optimal foraging, not biogenetic law, predicts spider orb web allometry

The biogenetic law posits that the ontogeny of an organism recapitulates the pattern of evolutionary changes. Morphological evidence has offered some support for, but also considerable evidence against, the hypothesis. However, biogenetic law in behavior remains underexplored. As physical manifestation of behavior, spider webs offer an interesting model for the study of ontogenetic behavioral changes. In orb-weaving spiders, web symmetry often gets distorted through ontogeny, and these changes have been interpreted to reflect the biogenetic law. Here, we test the biogenetic law hypothesis against the alternative, the optimal foraging hypothesis, by studying the allometry in Leucauge venusta orb webs. These webs range in inclination from vertical through tilted to horizontal; biogenetic law predicts that allometry relates to ontogenetic stage, whereas optimal foraging predicts that allometry relates to gravity. Specifically, pronounced asymmetry should only be seen in vertical webs under optimal foraging theory. We show that, through ontogeny, vertical webs in L. venusta become more asymmetrical in contrast to tilted and horizontal webs. Biogenetic law thus cannot explain L. venusta web allometry, but our results instead support optimization of foraging area in response to spider size.

[1]  S. Gould Ontogeny and phylogeny--revisited and reunited. , 1992, BioEssays : news and reviews in molecular, cellular and developmental biology.

[2]  S. Benjamin,et al.  Homology, behaviour and spider webs: web construction behaviour of Linyphia hortensis and L. triangularis (Araneae: Linyphiidae) and its evolutionary significance , 2004, Journal of evolutionary biology.

[3]  William G. Eberhard,et al.  Function and Phylogeny of Spider Webs , 1990 .

[4]  A. J. Moffat,et al.  A functional explanation of top-bottom asymmetry in vertical orbwebs , 1983, Animal Behaviour.

[5]  H. Peters Studien am netz der kreuzspinne (Aranea Diadema L.) , 1937, Zeitschrift für Morphologie und Ökologie der Tiere.

[6]  Kensuke Nakata,et al.  Upside-down spiders build upside-down orb webs: web asymmetry, spider orientation and running speed in Cyclosa , 2010, Proceedings of the Royal Society B: Biological Sciences.

[7]  J. Coddington,et al.  Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneoidea) , 1998 .

[8]  Samuel Zschokke,et al.  Spider orientation and hub position in orb webs , 2009, Naturwissenschaften.

[9]  Fritz Vollrath,et al.  Web construction patterns in a range of orb weaving spiders (Araneae) , 2013 .

[10]  Samuel Venner,et al.  Spider webs designed for rare but life-saving catches , 2005, Proceedings of the Royal Society B: Biological Sciences.

[11]  M. Kuntner,et al.  Ladder webs in orb-web spiders: ontogenetic and evolutionary patterns in Nephilidae , 2010 .

[12]  F. Vollrath,et al.  The Role of Behavior in the Evolution of Spiders, Silks, and Webs , 2007 .

[13]  M. Kuntner,et al.  Phylogeny accurately predicts behaviour in Indian Ocean Clitaetra spiders (Araneae : Nephilidae) , 2009 .

[14]  S. Zschokke,et al.  Asymmetry in Orb-Webs: An Adaptation to Web Building Costs? , 2008, Journal of Insect Behavior.

[15]  A. Sensenig,et al.  Webs in vitro and in vivo: spiders alter their orb-web spinning behavior in the laboratory , 2010 .

[16]  Jonathan A Coddington,et al.  Reconstructing web evolution and spider diversification in the molecular era , 2009, Proceedings of the National Academy of Sciences.

[17]  W. Shear,et al.  Spiders : webs, behavior, and evolution , 1986 .

[18]  J. Coddington The Monophyletic Origin of the Orb Web , 1986 .

[19]  M. F. Mickevich,et al.  Evolution of Chesapecten (Mollusca: Bivalvia, Miocene-Pliocene) and the Biogenetic Law , 1982 .

[20]  H. Saedler,et al.  MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. , 1995, Current opinion in genetics & development.

[21]  W. Eberhard The “Sawtoothed” Orb Web of Eustala Sp. (Araneae, Araneidae) with a Discussion of Ontogenetic Changes in Spiders' Web-Building Behavior , 1985 .

[22]  Andy P. Field,et al.  Discovering Statistics Using SPSS , 2000 .

[23]  M. Herberstein,et al.  Asymmetry in spider orb webs: a result of physical constraints? , 1999, Animal Behaviour.

[24]  Fritz Vollrath,et al.  Design features of the orb web of the spider, Araneus diadematus , 1994 .

[25]  M. Herberstein,et al.  Taking it to extremes: what drives extreme web elongation in Australian ladder web spiders (Araneidae: Telaprocera maudae)? , 2009, Animal Behaviour.

[26]  M. Herberstein,et al.  The role of experience in web-building spiders (Araneidae) , 1999, Animal Cognition.

[27]  W. Eberhard,et al.  Vestiges of an orb-weaving ancestor? The “biogenetic law” and ontogenetic changes in the webs and building behavior of the black widow spider Latrodectus geometricus (Araneae Theridiidae) , 2008 .

[28]  Thomas Hesselberg,et al.  Ontogenetic Changes in Web Design in Two Orb‐Web Spiders , 2010 .

[29]  M. Herberstein,et al.  Spider Behaviour: Flexibility And Versatility , 2011 .

[30]  Kensuke Nakata Does ontogenetic change in orb web asymmetry reflect biogenetic law? , 2010, Naturwissenschaften.

[31]  J. Wenzel Application of the biogenetic law to behavioral ontogeny: a test using nest architecture in paper wasps , 1993 .

[32]  A. Blejec,et al.  Ecology and web allometry of Clitaetra irenae, an arboricolous African orb-weaving spider (Araneae, Araneoidea, Nephilidae) , 2008 .

[33]  Ingi Agnarsson,et al.  The Form and Function of Spider Orb Webs: Evolution from Silk to Ecosystems , 2011 .

[34]  W. Eberhard The ‘inverted ladder’ orb web of Scoloderus sp. and the intermediate orb of Eustala (?) sp. Araneae: Araneidae , 1975 .

[35]  M. Herberstein,et al.  Spider webs: Evolution, diversity and plasticity , 2011 .

[36]  James Hanken,et al.  There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development , 1997, Anatomy and Embryology.

[37]  Lennart Olsson,et al.  Evolutionary developmental biology: its concepts and history with a focus on Russian and German contributions , 2010, Naturwissenschaften.

[38]  M. Richardson,et al.  Haeckel's ABC of evolution and development , 2002, Biological reviews of the Cambridge Philosophical Society.

[39]  C. Hayashi,et al.  Silk Genes Support the Single Origin of Orb Webs , 2006, Science.

[40]  G. Nelson Ontogeny, Phylogeny, Paleontology, and the Biogenetic Law , 1978 .

[41]  S. Gould Roots: Ontogeny and phylogeny – revisited and reunited , 1992 .

[42]  T. Blackledge Prey capture in orb weaving spiders: are we using the best metric? , 2011 .

[43]  Daiqin Li,et al.  Mass predicts web asymmetry in Nephila spiders , 2010, Naturwissenschaften.