Abstract
While niche construction theory locates animal artefacts in their constructors’ environment, hence treating them as capable of exerting selective pressure on both the constructors and their descendants, the extended phenotype concept assimilates artefacts with their constructors’ genes. Analogous contrasts apply in the case of endoparasite and brood parasite genes influencing host behaviour. The explanatory power of these competing approaches are assessed by re-examining the core chapters of Richard Dawkins’ The Extended Phenotype. Because animal artefacts (chapter 11) have multiple evolutionary consequences for their constructors, the extra-body effects of a gene seemingly include feedback effects on multiple other genes, a result which is more consistent with niche construction theory than with selfish gene theory. In the case of endoparasite genes influencing host behaviour (chapter 12), Dawkins’ argument leaves out what appears to be the key explanatory component, namely the role of the host’s own bodily systems in making it possible for such genes to exist. For action at a distance (chapter 13), it is unclear whether the key genes have extended effects because they sit in the body of the manipulating organism, or alternatively do not have such effects because they sit in the body of its victim. It is argued that niche construction theory offers a superior explanation in all three cases, regardless of whether the extended phenotype concept is interpreted in selfish gene or selfish organism terms.
Similar content being viewed by others
References
Adamo SA (2002) Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav Evol 60:370–377
Alatalo R, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323:152–153
Arvidsson B, Neergaard R (1991) Mate choice in the willow warbler—a field experiment. Behav Ecol Sociobiol 29:225–229
Bessert ML, Brozek J, Orti G (2007) Impact of nest substrate limitations on patterns of illegitimacy in the fathead minnow, Pimephales promelas (Cypriniformes: Cyprinidae). J Hered 98:716–722
Biron DG, Ponton F, Marche L, Galeotti N, Renault L, Demey-Thomas E, Poncet J, Brown SP, Jouin P, Thomas F (2006) ‘Suicide’ of crickets harbouring hairworms: a proteomics investigation. Insect Mol Biol 15:731–742
Brennan PA (2004) The nose knows who’s who: chemosensory individuality and mate recognition in mice. Horm Behav 46:231–240
Brooks DR, McLennan DA (1993) Macroevolutionary patterns of morphological diversification among parasitic flatworms (Platyhelminthes, Cercomeria). Evolution 47:495–509
Brown SP (2005) Do all parasites manipulate their hosts? Behav Process 68:237–240
Brown CR, Brown MB (1992) Ectoparasitism as a cause of natal dispersal in cliff swallows. Ecology 73:1718–1723
Brown SP, Le Chat L, Taddei F (2008) Evolution of virulence: triggering host inflammation allows invading pathogens to exclude competitors. Ecol Lett 11:44–51
Cezilly F, Perrot-Minnot MJ (2005) Studying adaptive changes in the behaviour of infected hosts: a long and winding road. Behav Process 68:223–228
Combes C (2005) Manipulations: variations on the themes of signalling and exaptation. Behav Process 68:211–213
Combes C, Morand S (1999) Do parasites live in extreme environments? Constructing hostile niches and living in them. Parasitology 119:S107–S110
Curtis LA (1990) Parasitism and the movements of intertidal gastropod individuals. Biol Bull 179:105–112
Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14
Dawkins R (1989) The selfish gene. Oxford University Press, Oxford
Dawkins R (1999) The extended phenotype: the long reach of the gene, Revised edn. Oxford University Press, Oxford
Dawkins R (2004) Extended phenotype—but not too extended. A reply to Laland, Turner and Jablonka. Biol Philos 19:377–396
deCatanzaro D (2011) Blastocyst implantation is vulnerable to stress-induced rises in endogenous estrogens and also to excretions of estrogens by proximate males. J Reprod Immunol 90:14–20
Deeming D (2002) Importance and evolution of incubation in avian reproduction. In: Deeming D (ed) Avian incubation: behaviour, environment and evolution. Oxford University Press, Oxford
Doerr NR (2012) Male great bowerbirds accumulate decorations to reduce the annual costs of signal production. Anim Behav 83:1477–1482
Eckerle K, Thompson C (2006) Mate choice in house wrens: nest cavities trump male characteristics. Behaviour 143:253–271
Fellows HL, Fenner AL, Bull CM (2009) Spiders provide important resources for an endangered lizard. J Zool 279:156–163
Gorelik G, Shackelford TK, Salmon CA (2010) New horizons in the evolutionary science of the human family. Rev Gen Psychol 14:330–339
Haig D (2012) The strategic gene. Biol Philos 27:461–479
Hammerschmidt K, Kurtz J (2009) Ecological immunology of a tapeworm’s interaction with its two consecutive hosts. Adv Parasitol 68:111–137
Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge
Hansell M, Deeming D (2002) Location, structure and function of incubation sites. In: Deeming D (ed) Avian incubation: behaviour, environment and evolution. Oxford University Press, Oxford
Helluy S, Holmes JC (2005) Parasitic manipulation: further considerations. Behav Process 68:205–210
Humphries S, Ruxton GD (1999) Bower-building: coevolution of display traits in response to the costs of female choice? Ecol Lett 2:404–413
Jones D (1990) Social organization and sexual interactions in Australian brush-turkeys (Alectura lathami): implications of promiscuity in a mound-building megapode. Ethology 84:89–104
Jones D, Dekker R, Roselaar C (1995) The megapodes. Oxford University Press, Oxford
Kavaliers M, Colwell DD (1995) Exposure to stable flies reduces spatial-learning in mice—involvement of endogenous opioid systems. Med Vet Entomol 9:300–306
Khan RA (1988) Experimental transmission, development, and effects of a parasitic copepod, Lernaeocera branchialis, on Atlantic cod, Gadus-morhua. J Parasitol 74:586–599
Labov JB (1981) Pregnancy blocking in rodents—adaptive advantages for females. Am Nat 118:361–371
Laland K (2004) Extending the extended phenotype. Biol Philos 19:313–325
Laland K, Sterelny K (2006) Seven reasons (not) to neglect niche construction. Evolution 60:1751–1762
Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proc Natl Acad Sci USA 96:10242–10247
Laland K, Odling-Smee J, Hoppitt W, Uller T (2013) More on how and why: cause and effect in biology revisited. Biology and Philosophy 28:719–745
Lefevre T, Adamo S, Biron D, Misse D, Hughes D, Thomas F (2009) Invasion of the body-snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Adv Parasitol 68:45–83
Lindström K, St. Mary C, Pampoulie C (2006) Sexual selection for male parental care in the sand goby, Pomatoschistus minutus. Behav Ecol Sociobiol 60:46–51
Mitchell N (2001) Males call more from wetter nests: effects of substrate water potential on reproductive behaviours of terrestrial toadlets. Proc R Soc Ser B 268:87–93
Moller AP (1991) Parasite load reduces song output in a passerine bird. Anim Behav 41:723–730
Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford
Morrell LJ, Hentley WT, Wickens VJ, Wickens JB, Rodgers GM (2012) Artificial enhancement of an extended phenotype signal increases investment in courtship by three-spined sticklebacks. Anim Behav 84:93–101
Odling-Smee J, Laland K, Feldman M (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton
Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. In: Brockmann H (ed) Advances in the study of behavior. Academic Press, Burlington, pp 151–186
Poulin R, Fitzgerald GJ (1989) Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can J Zool 67:14–18
Roberts EK, Lu A, Bergman TJ, Beehner JC (2012) A Bruce effect in wild geladas. Science 335:1222–1225
Schaedelin FC, Taborsky M (2009) Extended phenotypes as signals. Biol Rev 84:293–313
Schaedelin FC, Taborsky M (2010) Female choice of a non-bodily ornament: an experimental study of cichlid sand craters in Cyathopharynx furcifer. Behav Ecol Sociobiol 64:1437–1447
Schwagmeyer P (1979) The Bruce effect: an evaluation of male/female advantages. Am Nat 114:932–938
Scott-Phillips TC, Laland KN, Shuker DM, Dickins TE, West SA (2014) The niche construction perspective: a critical appraisal. Evolution 68:1231–1243
Sergio F, Blas J, Blanco G, Tanferna A, Lopez L, Lemus JA, Hiraldo F (2011) Raptor nest decorations are a reliable threat against conspecifics. Science 331:327–330
Seymour R (1985) Physiology of megapode eggs and incubation mounds. In: Acta XZIII Congressus Internationalis Ornithologici, vol 2. Nauka, Moscow, pp 854–863
Sorci G, Massot M, Clobert J (1994) Maternal parasite load increases sprint speed and philopatry in female offspring of the common lizard. Am Nat 144:153–164
Sterelny K (2005) Made by each other: organisms and their environment. Biol Philos 20:21–36
Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199
Tibbetts EA, Shorter JR (2009) How do fighting ability and nest value influence usurpation contests in Polistes wasps? Behav Ecol Sociobiol 63:1377–1385
Turner J (2004) Extended phenotypes and extended organisms. Biol Philos 19:327–352
Walter A, Elgar MA (2012) The evolution of novel animal signals: silk decorations as a model system. Biol Rev 87:686–700
Welch KA, Stanfield AC, Moorhead TW, Haga K, Owens DCG, Lawrie SM, Johnstone EC (2010) Amygdala volume in a population with special educational needs at high risk of schizophrenia. Psychol Med 40:945–954
Wells D (2012) Mating behaviour of the Australian brush-turkey. Dissertation, Macquarie University, Sydney
Zobel MU, Paxton RJ (2007) Is big the best? Queen size, usurpation and nest closure in a primitively eusocial sweat bee (Lasioglossum malachurum). Behav Ecol Sociobiol 61:435–447
Acknowledgments
I am grateful to Kevin Laland, Michael Gillings and Culum Brown for helpful comments on an earlier draft of this article.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wells, D.A. The extended phenotype(s): a comparison with niche construction theory. Biol Philos 30, 547–567 (2015). https://doi.org/10.1007/s10539-015-9476-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10539-015-9476-0