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Scaffolded biology

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Abstract

Descriptions and interpretations of the natural world are dominated by dichotomies such as organism vs. environment, nature vs. nurture, genetic vs. epigenetic, but in the last couple of decades strong dissatisfaction with those partitions has been repeatedly voiced and a number of alternative perspectives have been suggested, from perspectives such as Dawkins’ extended phenotype, Turner’s extended organism, Oyama’s Developmental Systems Theory and Odling-Smee’s niche construction theory. Last in time is the description of biological phenomena in terms of hybrids between an organism (scaffolded system) and a living or non-living scaffold, forming unit systems to study processes such as reproduction and development. As scaffold, eventually, we can define any resource used by the biological system, especially in development and reproduction, without incorporating it as happens in the case of resources fueling metabolism. Addressing biological systems as functionally scaffolded systems may help pointing to functional relationships that can impart temporal marking to the developmental process and thus explain its irreversibility; revisiting the boundary between development and metabolism and also regeneration phenomena, by suggesting a conceptual framework within which to investigate phenomena of regular hypermorphic regeneration such as characteristic of deer antlers; fixing a periodization of development in terms of the times at which a scaffolding relationship begins or is terminated; and promoting plant galls to legitimate study objects of developmental biology.

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References

  • Alegado RA, Brown LW, Cao S, Dermenjian RK, Zuzow R, Fairclough SR, Clardy J, King N (2012) A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1:e00013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Allen C (2014) Symbols as scaffolding. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 231–247

    Google Scholar 

  • Beck SD (1971) Growth and retrogression in larvae of Trogoderma glabrum (Coleoptera: Dermestidae). 1. Characteristics under feeding and starvation conditions. Ann Entomol Soc Am 64:149–155

    Article  Google Scholar 

  • Bickhard MH (1992) Scaffolding and self scaffolding: central aspects of development. In: Winegar LT, Valsiner J (eds) Children’s development within social contexts: research and methodology. Erlbaum, Hillsdale, pp 33–52

    Google Scholar 

  • Bickhard MH (2005) Functional scaffolding and self-scaffolding. New Ideas Psychol 23:166–173

    Article  Google Scholar 

  • Blackburn DG (1992) Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Am Zool 32:313–321

    Article  Google Scholar 

  • Blackburn DG (2000) Classification of the reproductive patterns of amniotes. Herpetol Monogr 14:371–377

    Article  Google Scholar 

  • Blackburn DG (2015) Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J Morphol 276:961–990

    Article  PubMed  Google Scholar 

  • Bosch TC, McFall-Ngai M (2011) Metaorganisms as the new frontier. Zoology 114:185–190

    Article  PubMed  PubMed Central  Google Scholar 

  • Callebaut W, Rasskin-Gutman D (eds) (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge

    Google Scholar 

  • Caporael LR (2001) Parts and wholes. The evolutionary importance of groups. In: Sedikides C, Brewer MB (eds) Individual self, relational self, and collective self: partners, opponents or strangers?. Psychology Press, Philadelphia, pp 241–253

    Google Scholar 

  • Caporael LR (2014) Evolution, groups, and scaffolded minds. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 57–76

    Google Scholar 

  • Caporael LR, Griesemer JR, Wimsatt WC (2014) Developing scaffolds in evolution, culture, and cognition. MIT Press, Cambridge

    Google Scholar 

  • Carneiro RG, Isaias RMS (2015) Gradients of metabolic accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking-insects. AoB Plants 7:plv086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carpenter JM, Perera EP (2006) Phylogenetic relationships among yellowjackets and the evolution of social parasitism. Am Mus Novit 3507:1–19

    Article  Google Scholar 

  • Carpenter JM, Strassmann JE, Turillazzi S, Hughes CR, Solis CR, Cervo R (1993) Phylogenetic relationships among paper wasp social parasites and their hosts (Hymenoptera: Vespidae). Cladistics 9:129–146

    Article  Google Scholar 

  • Chiu L, Gilbert SF (2015) The birth of the holobiont: multi-species birthing through mutual scaffolding and niche construction. Biosemiotics 8:191–210

    Article  Google Scholar 

  • Czechowski W (1990) A raid of Formica sanguinea Latr (Hymenoptera, Formicidae) on a conspecific colony. Memorab Zool 44:65–69

    Google Scholar 

  • Dawkins R (1982) The extended phenotype. WH Freeman, Oxford

    Google Scholar 

  • Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Boulétreau M (2001) Removing symbiotic Wolbachia specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Toro-De León G, García-Aguilar M, Gillmor CS (2014) Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514:624–627

    Article  PubMed  CAS  Google Scholar 

  • Drago L, Fusco G, Minelli A (2008) Non-systemic metamorphosis in male millipede appendages: long delayed, reversible effect of an early localized positional marker? Front Zool 5:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Drago L, Fusco G, Garollo E, Minelli A (2011) Structural aspects of leg-to-gonopod metamorphosis in male helminthomorph millipedes (Diplopoda). Front Zool 8:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmikophilen Ameisen. Biol Cbl 29:352–362

    Google Scholar 

  • Evans JA (2014) Communication and the evolution of cognition. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 125–146

    Google Scholar 

  • Felt EP (1940) Plant galls and gall-makers. Comstock, Ithaca

    Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gadau J, Strehl C-P, Oettler J, Hölldobler B (2003) Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids. Mol Ecol 12:1931–1938

    Article  CAS  PubMed  Google Scholar 

  • Gerson EM (2014) Some problems of analyzing cultural evolution. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 265–281

    Google Scholar 

  • Gilbert SF, Bosch TCG, Ledón-Rettig C (2015) Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat Rev Genet 16:611–622

    Article  CAS  PubMed  Google Scholar 

  • Griesemer J (2007) Tracking organic processes. Representations and research styles in classical embryology and genetics. In: Laubichler MD, Maienschein J (eds) From embryology to evo-devo. A history of developmental evolution. MIT Press, Cambridge, p 375–433

    Google Scholar 

  • Griesemer JR (2014a) Reproduction and scaffolded developmental processes: an integrated evolutionary perspective. In: Minelli A, Pradeu T (eds) Towards a theory of development. Oxford University Press, Oxford, pp 183–202

    Chapter  Google Scholar 

  • Griesemer JR (2014b) Reproduction and the scaffolded development of hybrids. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 23–55

    Google Scholar 

  • Griesemer JR, Caporael LR, Wimsatt WC (2014) Developing scaffolds: an epilogue. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 363–388

    Google Scholar 

  • Griffiths PE, Gray RD (1994) Developmental systems and evolutionary explanation. J Philos 91:277–304

    Article  Google Scholar 

  • Griffiths PE, Gray RD (2001) Darwinism and developmental systems. In: Oyama S, Griffiths PE, Gray RD (eds) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge, pp 195–218

    Google Scholar 

  • Griffiths PE, Gray RD (2004) The developmental systems perspective: organism–environment systems as units of evolution. In: Preston K, Pigliucci M (eds) The evolutionary biology of complex phenotypes. Oxford University Press, Oxford, pp 409–431

    Google Scholar 

  • Griffiths PE, Gray RD (2005) Discussion: three ways to misunderstand developmental systems theory. Biol Philos 20:417–425

    Article  Google Scholar 

  • Hadfield MG (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Ann Rev Mar Sci 3:453–470

    Article  PubMed  Google Scholar 

  • Hall BK (1999) The neural crest in development and evolution. Springer, New York

    Book  Google Scholar 

  • Heintz C (2014) Scaffolding on core cognition. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 209–228

    Google Scholar 

  • Hoerauf A (2008) Mansonella perstans—the importance of an endosymbiont. N Engl J Med 361:1502–1504

    Article  Google Scholar 

  • Hölldobler B (1976) Tournaments and slavery in a desert ant. Science 192:912–914

    Article  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Horberg Wimsatt B (2014) Footholds and handholds: scaffolding cognition and career. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 343–362

    Google Scholar 

  • Jost J (2014) Obituary for Olaf Breidbach. Theory Biosci 133:125–128

    Article  PubMed  Google Scholar 

  • Katada S, Imhof A, Sassone-Corsi P (2012) Connecting threads: epigenetics and metabolism. Cell 148:24–28

    Article  CAS  PubMed  Google Scholar 

  • Kostoff D, Kendall J (1929) Studies on the structure and development of certain cynipid galls. Biol Bull 56:402–458

    Article  Google Scholar 

  • Kronauer DJC, Gadau J, Hölldobler B (2003) Genetic evidence for intra- and interspecific slavery in honey ants (genus Myrmecocystus). P R Soc Lond B 270:805–810

    Article  CAS  Google Scholar 

  • La Barre S (2011) Coral reef biodiversity in the face of climatic changes. In: Grillo O (ed) Biodiversity series, book 4. Biodiversity loss in a changing planet. Intech, Croatia

    Google Scholar 

  • Laland KN, Odling-Smee FJ, Turner S (2014) The role of internal and external constructive processes in evolution. J Physiol 592:2413–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landmann F, Foster JM, Michalski ML, Slatko BE, Sullivan W (2014) Coevolution between an endosymbiont and its nematode host: Wolbachia asymmetric posterior localization and AP polarity establishment. PLoS Negl Trop Dis 8:e3096

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Douarin N (1982) The neural crest. Cambridge University Press, Cambridge

    Google Scholar 

  • Le Moli F, Grasso DA, D’Ettorre P, Mori A (1993) Intraspecific slavery in Polyergus rufescens Latr. (Hymenoptera, Formicidae): field and laboratory observations. Insect Soc 40:433–437

    Article  Google Scholar 

  • Lewontin RC (1982) Organism and environment. In: Plotkin HC (ed) Learning, development, culture. Wiley, Chichester, pp 151–170

    Google Scholar 

  • Lewontin RC (1983a) Gene, organism, environment. In: Bendall DS (ed) Evolution: from molecules to man. Cambridge University Press, Cambridge, pp 273–285

    Google Scholar 

  • Lewontin RC (1983b) The organism as the subject and object of evolution. Scientia 118:65–82

    Google Scholar 

  • Li S-C (2014) Biocultural coconstruction of brain plasticity across the life span: from cognitive training to neurotransmitters. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 327–342

    Google Scholar 

  • Lopez-Vaamonde C, Koning JW, Brown RM, Jordon WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560

    Article  CAS  PubMed  Google Scholar 

  • Lyon P (2014) Stress in mind: a stress response hypothesis of cognitive evolution. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 171–190

    Google Scholar 

  • Mantovani B, Scali V (1992) Hybridogenesis and androgenesis in the stick-insect Bacillus rossius-grandii benazzii (Insecta, Phasmatodea). Evolution 46:783–796

    Article  Google Scholar 

  • Martínez SF (2014) Technological scaffoldings for the evolution of culture and cognition. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 249–263

    Google Scholar 

  • Mendel G (1866) Versuche über Pflanzen-Hybriden. Verh Naturforsch Ver Abh Brünn 4:3–47

    Google Scholar 

  • Minelli A (2003) The development of animal form: ontogeny, morphology, and evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Minelli A (2011) A principle of developmental inertia. In: Hallgrímsson B, Hall BK (eds) Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, San Francisco, pp 116–133

    Google Scholar 

  • Minelli A (2014) Developmental disparity. In: Minelli A, Pradeu T (eds) Towards a theory of development. Oxford University Press, Oxford, pp 227–245

    Chapter  Google Scholar 

  • Minelli A (2015) Grand challenges in evolutionary developmental biology. Front Ecol Evol 2:85

    Article  Google Scholar 

  • Minelli A, Pradeu T (2014) (eds) Towards a theory of development. Oxford University Press, Oxford

  • Murmann JP (2014) Scaffolding in economics, management, and the design of technologies. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 287–305

    Google Scholar 

  • Nacoulma AP, Vandeputte OM, De Lorenzi M, El Jaziri M, Duez P (2013) Metabolomic-based study of the leafy gall, the ecological niche of the phytopathogen Rhodococcus fascians, as a potential source of bioactive compounds. Int J Mol Sci 14:12533–12549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Newman SA (2014) Excitable media in medias res: how physics scaffolds metazoan development and evolution. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 109–123

    Google Scholar 

  • Odling-Smee FJ (1988) Niche-constructing phenotypes. In: Plotkin HC (ed) The role of behavior in evolution. MIT Press, Cambridge, pp 73–132

    Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Ostrovsky AN, Lidgard S, Gordon DP, Schwaha T, Genikhovich G, Ereskovsky AV (2015) Matrotrophy and placentation in invertebrates: a new paradigm. Biol Rev. doi:10.1111/brv.12189

    PubMed  Google Scholar 

  • Oyama S (1985) The ontogeny of information: developmental systems and evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Oyama S, Griffiths PE, Gray RD (eds) (2001) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge

    Google Scholar 

  • Pamilo P, Pekkarinen A, Varvio-Aho S-L (1987) Clustering of bumblebee subgenera based on interspecific genetic relationships (Hymenoptera, Apidae: Bombus and Psithyrus). Ann Zool Fenn 24:19–27

    Google Scholar 

  • Pietsch TW (2005) Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes). Ichthyol Res 52:207–236

    Article  Google Scholar 

  • Pitts JP, McHugh JV, Ross KG (2005) Cladistic analysis of the fire ants of the Solenopsis saevissima species-group (Hymenoptera: Formicidae). Zool Scr 34:493–505

    Article  Google Scholar 

  • Plowright RC, Stephen WP (1973) A numerical taxonomic analysis of the evolutionary relationships of Bombus and Psithyrus (Apidae: Hymenoptera). Can Entomol 105:733–743

    Article  Google Scholar 

  • Poinar GOJ, van der Laan PA (1972) Morphology and life history of Sphaerularia bombi. Nematology 18:239–252

    Article  Google Scholar 

  • Raff RA, Sly BJ (2000) Modularity and dissociation in the evolution of gene expression territories in development. Evol Dev 2:102–113

    Article  CAS  PubMed  Google Scholar 

  • Ramos GC (2012) Inflammation as an animal development phenomenon. Clin Dev Immunol. Article ID 983203

  • Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  • Ross H (1911) Die Pflanzengallen (Cecidien) Mittel- und Nordeuropas, ihre Erreger und Biologie und Bestimmungstabellen. Fischer, Jena

    Google Scholar 

  • Rouse GW, Goffredi SK, Vrijenhoek RC (2004) Osedax: bone-eating marine worms with dwarf males. Science 305:668–671

    Article  CAS  PubMed  Google Scholar 

  • Sassone-Corsi P (2013) When metabolism and epigenetics converge. Science 339:148–150

    Article  CAS  PubMed  Google Scholar 

  • Savolainen R, Vepsäläinen K (2003) Sympatric speciation through intraspecific social parasitism. Proc Natl Acad Sci USA 100:7169–7174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scali V, Passamonti M, Marescalchi O, Mantovani B (2003) Linkage between sexual and asexual lineages: genome evolution in Bacillus stick insects. Biol J Linn Soc 79:137–150

    Article  Google Scholar 

  • Schank JC, May CJ, Joshi SS (2014) Models as scaffolds for understanding. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, MA, pp 147–167

    Google Scholar 

  • Schlosser G, Wagner GP (2004) Modularity in development and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Schumann RD (1992) Raiding behavior of the dulotic ant Chalepoxenus muellerianus (Finzi) in the field (Hymenoptera: Formicidae, Myrmicinae). Ins Soc 39:325–333

    Article  Google Scholar 

  • Stotz K (2008) The ingredients for a postgenomic synthesis of nature and nurture. Philos Psychol 21:359–381

    Article  Google Scholar 

  • Sumner S, Aanen DK, Delabie J, Boomsma JJ (2004) The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Ins Soc 51:37–42

    Article  Google Scholar 

  • Tavory I, Ginsburg S, Jablonka E (2014) The reproduction of the social: a developmental system approach. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 307–325

    Google Scholar 

  • Theiner G (2014) Onwards and upwards with the extended mind: from individual to collective epistemic action. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 191–208

    Google Scholar 

  • Turner JS (2000) The extended organism: the physiology of animal-built structures. Harvard University Press, Cambridge

    Google Scholar 

  • Uzzell T, Günther R, Berger L (1977) Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proc Acad Nat Sci Phila 128:147–171

    Google Scholar 

  • von Siebold CT (1851) Über die conjugation des Diplozoon paradoxum. Ztsch wiss Zool 3:62–68

    Google Scholar 

  • Vrijenhoek RC (1994) Unisexual fish: model systems for studying ecology and evolution. Ann Rev Ecol Syst 25:71–96

    Article  Google Scholar 

  • Waterman RJ, Bidartando MI (2008) Deception above, deception below: linking pollination and mycorrhizal biology of orchids. J Exp Bot 59:1085–1096

    Article  CAS  PubMed  Google Scholar 

  • Williams PH (1985) A preliminary cladistic investigation of relationship among the bumble bees (Hymenoptera; Apidae). Syst Entomol 10:239–255

    Article  Google Scholar 

  • Wimsatt WC (2014) Entrenchment and scaffolding: an architecture for a theory of cultural change. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolding in evolution, cognition and culture. MIT Press, Cambridge, pp 77–105

    Google Scholar 

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Acknowledgments

I am grateful to Jürgen Jost for his invitation to contribute to this issue of Theory in Biosciences dedicated to the memory of Olaf Breidbach, to Giuseppe Fusco for his critical reading of the text and to the two referees for their insightful comments.

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  1. Department of Biology, University of Padova, Via Ugo Bassi 58 B, Padova, 35131, Italy

    Alessandro Minelli

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Correspondence to Alessandro Minelli.

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This article is dedicated to the memory of Olaf Breidbach—inspiring thinker, tireless researcher, dear friend.

This article forms part of a special issue of Theory in Biosciences in commemoration of Olaf Breidbach.

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Minelli, A. Scaffolded biology. Theory Biosci. 135, 163–173 (2016). https://doi.org/10.1007/s12064-016-0230-1

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