At the end of the eighteenth century, the French physician, Théophile de Bordeu, observed that the honeybee colony behaved in many ways like an organism. There was coordination among the worker bees, specialization, collective work, coherency, and something like a hive intelligence. What the coherent organism and the coherent honeybee colony had in common, Bordeu argued, was similarity in the process of ongoing negotiation and mutual accommodation—the workers in the case of the insect colony, the innumerable cells and organs in the case of the organism. A century later, Claude Bernard found himself drawn to this form of vitalism.1 Like Bordeau, he proposed to explain physiology by appealing to the ongoing negotiation and mutual accommodation between parts of an organism—its many little lives.

Fit or Foul

A  bird that is well-adapted to its environment uses energy and materials efficiently. The better adapted the bird, the fitter it is. A fitter fowl is a fecund fowl. This is the meaning of fitness. Fitness is continuous and progressive—progressive because birds living in a cold environment, say, tend over generations to develop a better-suited, a more apt, insulating plumage; and continuous because pigeons give rise to pigeons, and not hawks, and hawks give rise to hawks, and not pigeons. Heritability is an agent both of stasis and change.2 So much was clear to Charles Darwin in 1868. In The Variation of Animals and Plants under Domestication,3 he drew a distinction between hard and soft inheritance. Stasis is hard, a matter of one pigeon after the other; change is soft, a matter of those fitter fowls. But Darwin had no idea how any of this came about, and, in fact, committed himself to a blending theory of inheritance, which did not work and did no good. Gregor Mendel understood that generations could remain the same and change only if the mechanism of inheritance was discrete; it was Mendel who first worked out a statistical theory for how particles of hard inheritance, later called genes, were transmitted from generation to generation. Some thirty years later, August Weismann located the carriers of hard inheritance in the nucleus, specifically on the enigmatic threadlike bodies called chromosomes. By the 1920s, Thomas Hunt Morgan had reconciled certain contradictions between Mendel’s  atoms of heredity and Weismann’s chromosomal theory of hard inheritance. The way was open to the modern synthesis. Between roughly 1920 and 1950, Ronald Fisher, Sewall Wright and J. B. S. Haldane developed a statistical model of Mendelian genetics, showing mathematically how natural selection could work in combination with random mutations to bring about evolutionary change.

A Vicious Circle

It was Wright who in 1932 introduced biologists to the metaphor of a fitness landscape. The landscape itself consists of plateaus and mountains, whether steep or shallow. It is across such a landscape that lineages travel through time. Peaks correspond to combinations of genes that indicate fitness.4 The higher along a fitness landscape a lineage travels, the fitter its constituent organisms. This proved a remarkably fertile metaphor. In the 1950s, G. Evelyn Hutchinson recast Wright’s fitness landscape into a metaphor for ecological adaptation: organisms occupy niches of apt function. Ten years later, William Hamilton recast enlarged fitness to encompass inclusive fitness, which included the effects of selection on all carriers of a gene, not just the individual carrying it.5 Yet, Wright and Hamilton were both trapped in a vicious circle. If evolutionary adaptation is natural selection acting on the fitter genes, just what are the fitter genes? The unsatisfying answer is: those that are naturally selected.6

The same problem reoccurs when niches are considered. A niche can be identified by the existence of a species occupying it.7 Species occupy the niche through a process of natural selection. Thus, flying insectivores like bats or swifts exist because they have evolved adaptations to occupy the flying insectivore niche, which include high maneuverability in flight, some means of filtering insects from the air, and navigation through sound. Bats differ from swifts because they have evolved to split the flying insectivore niche into the daytime flying insectivore niche (swifts) and a nighttime flying insectivore niche (bats). Thus, niches proliferate ad hoc as need arises.

Wright himself was frank on this question: based upon his estimate that higher organisms could be specified by as many as a thousand different genes, he concluded that the number of possible gene combinations was essentially infinite.8 It is sobering to contemplate that Wright underestimated the number of functional genes in higher organisms by about an order of magnitude.9

How, then, to identify from that infinitude of gene combinations the adaptive peaks and differentiate them from the valleys and the flat plains? For the metaphor to become a predictive tool, there must be some filter that can independently identify an adaptive peak.

Such filters have proven hard to come by.10 The vicious circle remains unbroken.

A Virtuous Circle

Niche construction theory has offered biologists a way to transform a vicious into a virtuous circle.11 In the conventional Darwinian view, organisms adapt to an environment that exists independently of the organism. The organism either fits in the environment or it does not. Fit organisms thus reproduce where less fit organisms do not, or at least not so fruitfully. “The organism proposes, and the environment disposes,” as Richard Lewontin famously put it.12 The interaction between organism and environment is not one-sided. Organisms routinely modify their environments. Adaptation is a two-way street.13 Beavers build impoundment dams to promote the growth of their favored food, birds build nests for shelter, desiccation-prone earthworms create moist and aerated soils. Examples are not simply numerous, but ubiquitous.14

This notion of reciprocal adaptation opens the door to reunifying evolutionary adaptation and physiological adaptation. Organisms make environments function well for themselves.15 Adaptation is a form of purposeful agency.

And agency operates in niche construction theory by means of the extended organism.16 Conceived independently of niche construction theory, the extended organism idea recasts adaptation as a phenomenon of adaptive boundaries. Adaptive boundaries partition environments, and they come in a variety of forms: cell membranes (partitioning the cytoplasm from the surroundings), epithelia (separating environments within the organs of the body), skins (which separate the organism from its environment), and environments (which can be subdivided at scales that are limited only by the extent of the biosphere).

The adaptive boundary works to sustain the environment contained within it, through managing flows of matter and energy across the boundary. To give an example, cells commonly maintain a high concentration of potassium ions in their cytoplasm. To do so, proteins embedded within the cell membrane do metabolic work to pump potassium into the cell, elevating its concentration there. At the same time, the membrane contains proteins that manage the leakage of potassium from the cell. The maintenance of high potassium in the cell is managed through a process that has been likened to keeping a leaky bucket full: potassium concentration in the cell is sustained by pumping potassium into the cell as fast as it leaks out. How rapidly the potassium leaks out is determined by the difference in concentration across the cell membrane—leakage rate will be faster in fresh water environments than they will be in saltier environments—and this determines the rate at which work must be done to pump the potassium back in. The cell membrane is an adaptive boundary because it adjusts pumping and leakage rates to sustain the cell’s internal potassium concentration over a range of possible environments.

Extended Physiology

As I have just described it, this is conventional physiology, but there is an unspoken assumption behind this description: that physiology is something that happens within an adaptive boundary. The concentration of potassium within the cell comes about through a process that depletes potassium beyond the cell. Both environments partitioned by the adaptive boundary of the cell membrane are affected, and physiology therefore cannot be something that operates strictly within the confines of the cell membrane. Physiology must be extended.

The extended organism idea follows. Adaptive boundaries can occur in a variety of forms. Cells, enveloped within their own adaptive boundaries of cell membrane, can enter coalitions to form sheets of cells, or epithelia, that also partition environments. Epithelia, in their turn, can enter larger coalitions to form organs, which can themselves cooperate to form organisms. Organisms, for their part, can modify environments to form new adaptive boundaries. Earthworms cooperate to build a soil environment that manages their water balance, so that the earthworm and earthworm-modified soil become an extended organism.17 At this point, the ideas of niche construction theory and the extended organism converge; the extended organism is the physiological manifestation of niche construction.18


The logic of extended physiology, as I have described it so far, is the logic of the machine. It is the logic of both the thermostat and the body. Yet, it contains the seeds of a radical challenge to the prevailing machine metaphor of life, and of the machine logic of modern Darwinism. Extended physiology points not just to the extended organism, but to organisms’ fundamental attribute of homeostasis: Claude Bernard’s signature idea. Extended physiology thus becomes extended homeostasis. Because extended physiology is equivalent to niche construction, extended homeostasis brings an adaptive dimension to niche construction theory in a way that makes evolution an explicitly purposeful and intention-driven phenomenon. Homeostasis is an evolutionary process in addition to a physiological one. Physiological and evolutionary adaptation are reunited.

A useful illustration: termites in southern Africa. These termite societies build massive mounds, which dot the landscape of the semi-arid savannas of sub-Saharan Africa. The termites that build these mounds can survive in much harsher conditions than other termite species. In the conventional Darwinian explanation, adaptation to hot and dry conditions occurs through the selection of genes for high tolerance of heat and desiccation. For some species of termites, this appears to have been precisely the case: the harvester termites that inhabit the same environments as the mound-building termites are active on the surface at all times of day.19 But mound-building termites are not especially tolerant of either high temperature or desiccation,20 yet they too live in extremely hot and dry environments.

What mound-building termites do is create an adapted environment by niche construction, or extended homeostasis. The colony does not live in the mound itself. Instead, their nests, of between one and two million individuals, are about a meter below the mound, where temperatures are less extreme. The termites also actively manage nest moisture. They construct water catchments between two and three meters below the nest, which impound the summer’s rainfalls. During the annual dry season, workers bring that cached water up, to offset water loss to the dry environment. During the rainy season, water infiltrating into the nest from torrential summer downpours make the nest too moist; wet soil is then carried up into the mound and deposited by the termites on the mound surface. The nest moisture thus remains roughly constant through the year, in the face of wide variation of moisture in the physical environment.

The extended homeostasis of the termite colony has set and driven their fitness milieu. Their evolution has been dominated by physiological, rather than genetic, factors. It is a common phenomenon in nature; life inexorably modifies the environment in which it is embedded.21

Where the idea of an extended organism gives adaptation and evolution a physiological dimension, extended homeostasis gives adaptation and evolution a cognitive dimension. Cognition is implicit in the phenomenon of homeostasis. The termites have some collective awareness of the condition of the nest—too wet, too dry, just right?—which in turn is cognitively mapped onto the collective swarm. Work is organized in order to adapt the environment: water brought into the nest, water exported from the nest, or water left as it is. Colony homeostasis is a phenomenon of a swarm-level cognition that is aware of conditions and undertakes work to sustain the nest environment in a state congenial to its inhabitants.22

Evolution enters the picture because the colony’s extended homeostasis has allowed these termites to extend their ranges into hotter and dryer conditions than they are genetically equipped to tolerate. They do so by actively controlling the fitness landscape. The extended organism is also an evolutionary concept; evolution is driven not by natural selection, but by extended homeostasis.

This is the radical implication of melding niche-construction theory with the idea of an extended organism. Fitness landscapes are shaped by purposeful manipulation of environments, through cognitive perception and striving of Bordeu’s many little lives. Genes become evolution’s lagging indicators, not its drivers. Life no longer evolves through genetic whimsy, but because, in a deep sense, life wants to evolve in a particular way.23

  1. Claude Bernard, An Introduction to the Study of Experimental Medicine (New York: Henry Schuman, 1865). 
  2. Peter Bowler, The Eclipse of Darwinism: Anti-Darwinian Evolution Theories in the Decades Around 1900 (Baltimore: Johns Hopkins University Press, 1983). 
  3. Charles Darwin, The Variation of Animals and Plants under Domestication (London: John Murray, 1868). 
  4. Massimo Pigliucci, “Sewall Wright’s Adaptive Landscapes: 1932 vs. 1988,” Biology and Philosophy 23, no. 5 (2008): 591–603, doi:10.1007/s10539-008-9124-z. 
  5. Richard Dawkins, The Selfish Gene (New York: Oxford University Press, 1976), 224. 
  6. Michael Rose and Laurence Mueller, Evolution and Ecology of the Organism (Upper Saddle River, NJ: Pearson Prentice Hall, 2006). 
  7. Robert Holt, “Bringing the Hutchinsonian Niche into the 21st Century: Ecological and Evolutionary Perspectives,” Proceedings of the National Academy of Sciences of the United States of America 106 (2009): 19,659–65, doi:10.1073/pnas.0905137106. 
  8. Massimo Pigliucci, “Sewall Wright’s Adaptive Landscapes: 1932 vs. 1988,” Biology and Philosophy 23, no. 5 (2008): 591–603, doi:10.1007/s10539-008-9124-z. 
  9. J. Craig Venter et al., “The Sequence of the Human Genome,” Science 291, no. 5,507 (2001): 1,304–51. 
  10. Jerry Coyne, Nicholas Barton, and Michael Turelli, “Perspective: A Critique of Sewall Wright’s Shifting Balance Theory of Evolution,” Evolution 51 (1997): 643–71, doi:10.2307/2411143; Jonathan Kaplan, “The End of the Adaptive Landscape Metaphor?” Biology and Philosophy 23, no. 5 (2008): 625–38, doi:10.1007/s10539-008-9116-z. 
  11. F. John Odling-Smee, Kevin Laland, and Marcus Feldman, “Niche Construction,” The American Naturalist 147, no. 4 (1996): 641–48. 
  12. Richard Lewontin, The Triple Helix: Gene, Organism and Environment (Cambridge, MA: Harvard University Press, 2000), 43. 
  13. Joseph Alper, “Ecosystem ‘Engineers’ Shape Habitats for Other Species,” Science 280, no. 5,367 (1998): 1,195–96; Clive Jones et al., “A Framework for Understanding Physical Ecosystem Engineering by Organisms,” Oikos 119, no. 12 (2010): 1862–69, doi:10.1111/j.1600-0706.2010.18782.x. 
  14. J. Scott Turner, The Extended Organism: The Physiology of Animal-Built Structures (Cambridge, MA: Harvard University Press, 2000). 
  15. J. Scott Turner, The Extended Organism: The Physiology of Animal-Built Structures (Cambridge, MA: Harvard University Press, 2000); J. Scott Turner, “Extended Phenotypes and Extended Organisms,” Biology and Philosophy 19 (2004): 327–52. 
  16. J. Scott Turner, The Extended Organism: The Physiology of Animal-Built Structures (Cambridge, MA: Harvard University Press, 2000). 
  17. J. Scott Turner, The Extended Organism: The Physiology of Animal-Built Structures (Cambridge, MA: Harvard University Press, 2000). 
  18. J. Scott Turner, “Homeostasis and the Physiological Dimension of Niche Construction Theory in Ecology and Evolution,” Ecology and Evolution 30 (2016): 203–19, doi:10.1007/s10682-015-9795-2. 
  19. Jannette Mitchell, P. H. Hewitt, and Theunis van der Linde, “Critical Thermal Limits and Temperature Tolerance in the Harvester Termite Hodotermes mossambicus (Hagen),” Journal of Insect Physiology 39 (1993): 523–28. 
  20. Faysal Tageldin Abushama, “Water-Relations of the Termites Macrotermes bellicosus (Smeathman) and Trinervitermes geminatus (Wasmann),” Zeitschrift für Angewandte Entomologie 75 (1974): 124–34, doi:10.1111/j.1439-0418.1974.tb01838.x. 
  21. J. Scott Turner, The Extended Organism: The Physiology of Animal-Built Structures (Cambridge, MA: Harvard University Press, 2000); J. Scott Turner, “Extended Phenotypes and Extended Organisms,” Biology and Philosophy 19 (2004): 327–52. 
  22. J. Scott Turner, “Termites as Models of Swarm Cognition,” Swarm Intelligence 5 (2011): 19–43, doi:10.1007/s11721-010-0049-1; J. Scott Turner et al., “Termites, Water and Soils,” Journal of the Agricultural Scientific Society of Namibia (2006): 40–45. 
  23. J Scott Turner, Purpose and Desire. What Makes Something “Alive” and Why Modern Darwinism Has Failed to Explain It (New York, New York: HarperOne, 2017).