Everything that happens has a cost. Physics treats this reality as a gigantic accounting system governed by the laws of thermodynamics. The most important of these laws is the second, which states that in all causal transformations, energy goes irreversibly from a higher to a lower state, or ability to do work. Irreversibility means energy-transforming systems have a sense of time, and can be said to be “making time” or “buying time.” The transactions can be measured in terms of the net transformation of energy (most easily seen as heat loss) or in terms of the movements of particles in the system affected by the transformation of energy (called statistical mechanics). No matter how these transformations manifest themselves, there is a net cost called “entropy.” So, another way to characterize the second law is to say that in every spontaneously occurring causal activity, entropy increases.
Traditional thermodynamics limited the energy account of a system. When energy levels inside a given system reached the same state as those outside the system, there could not be any more transformations. This is called “equilibrium.” It is the point at which the energy bank account has been exhausted, the system has achieved maximum entropy. Only if new energy of a higher grade than the surroundings is transferred into the system can it function again. Recognition of the implications of this version of the laws of thermodynamics caused panic and denial among many late nineteenth century physicists. Just as the Darwinian reality inspired “Nature red in tooth and claw,” thermodynamics inspired “Heat death of the universe.” To complete the circle, Ludwig von Boltzmann, a pioneer in statistical mechanics, gave a public lecture in Leipzig in 1905, proclaiming that Darwinian evolution was a statistical mechanical manifestation of the second law of thermodynamics.
Less than a decade later, Lotka (1913, 1925) became one of the first twentieth century authors to formally characterize biological systems as metabolic systems, maintaining themselves in highly organized states with respect to their environments by exchanging matter and energy irreversibly with their surroundings, taking in relatively high-grade energy and using it to perform useful work within the system. He suggested that the inevitable structural decay that accompanies such transactions could be delayed, although not reversed, by the system’s accumulation of energy from outside. Even here, organisms have a dual nature. Organisms undergo heat-generating transformations, involving a net loss of energy from the system, usually in the form of heat, and conservative transformations, involve changing free energy into states that can be stored and utilized in subsequent transformations. All conservative transformations in biological systems are coupled with heat generating transformations, but the reverse is not true; there is a heavy energetic cost to maintaining structure (Brooks et al. 1989; Brooks and McLennan 1990; Maurer and Brooks 1991).
Closed, or equilibrium, thermodynamic systems are a sort of WYSIWYG (what you see is what you get) system. Given a certain amount of matter and energy, the energy will be transformed to a lower state and the matter dispersed in its container as a result. Once the energy levels inside match the surroundings, and the matter inside is dispersed maximally given the boundaries of its container, equilibrium is reached and all work ceases. The bank account is empty, maximum entropy has been achieved. Equilibrium systems show no duality in energy use, so that framework clearly is inadequate for understanding biological systems.
Open, or nonequilibrium, systems allow new energy and matter to flow through, and so long as the flow continues the system functions. Total entropy changes (dS) in open systems (called entropy production because there is no a priori entropy maximum) are subdivided into exchanges between the system and its surroundings (deS: heat-generating transformations) and production internal to the system (d
i
S: conservative transformations). Exchanges between organisms and their surroundings cost a lot and are accompanied by much waste dissipated into the surroundings; hence, deS is large compared with d
i
S. However, open systems can maintain their structural integrity only by producing entropy internally (d
i
S > 0). Or,
Organismal production (d
i
S), manifested as information production, storage and transmission (biomass and inheritance), is critically important, even though it represents a tiny portion of an organism’s energy budget.
Biological systems maintain themselves in highly organized states far from thermodynamic equilibrium with respect to their environments through causal engagement with the surroundings, mediated by a “phase separation” (Prigogine 1980). That is, there is an “inside” and an “outside,” delineated by a physical boundary. For all organisms, this boundary is provided by cell membranes, which are simultaneously physical barriers between the inside and outside of the organism and highly selective mechanisms for modulating the exchange of matter and energy between the organism and its surroundings. For multicellular organisms, this barrier is a complex of cell membranes.
Production rules govern internal processes for which there is an energetic “cost” or “allocation.” Following Zotin and Zotina (1978), Brooks and Wiley (1988) used ψ to denote energy dissipation within the system. The function includes two major classes of processes: (1) the external dissipation function
, mostly heat generated by production within the organism and lost to the surroundings, adding to the energy lost as a result of bringing matter and usable energy into the system from the surroundings and (2) the bound dissipation function
, all structure maintained within the organism. In organisms,
can be further subdivided into allocations for accumulating biomass
and allocations for accumulating information that can be passed on by inheritance
. Thus, d
i
S can be viewed heuristically as
Heat-generating processes, deS and
, occur when energy and entropy flow in opposite directions, moving the system toward disordered states. Organisms slow these effects by “exporting” entropy to the surroundings; if all the heat generated by processes associated with bringing matter and energy into an organism stayed in the organism, it would rapidly die. Conservative transformations are characterized by energy and entropy flowing in the same direction, entropy production being retained within the system and tending to move the system toward more structured states. As entropy and energy flow through biological systems at different rates, structure accumulates at different levels of organization; furthermore, the structure at any given level is constrained by energy and entropy flows at other levels.
Organisms maintain themselves through time by exploiting “resource gradients” in the surroundings (Ulanowicz 1997), determined by interactions between abiotic and biotic factors. Abiotic factors can be structured in part by metabolic components of biological production
. For example, both the capture of incoming solar energy by organisms and their mass re-radiation of heat affect the thermal profile of the earth. Likewise, oxygen production as a byproduct of photosynthesis or of carbon dioxide as a byproduct of aerobic metabolism affect the composition of the earth’s atmosphere. More simply, production (d
i
S) can influence exchanges (deS). Biotic factors are also subject to the influences of the structural portion of biological production
. Metabolism tends to move biological systems in the direction of minimizing energy gradients in the environment, to the extent permitted by the inherited capabilities (and limitations) of the organisms involved (Ulanowicz 1997; Brooks and McLennan 2000). In other words, accumulated genetic information
constrains the patterns of energy flow
within organisms and between organisms and their surroundings (deS).
Biological systems produce entropy at different rates because energy stored by conservative transformations is degraded at different rates. At the lowest organizational levels, shortest time intervals, and smallest spatial scales, the greatest contribution to ψ is
. If we examine cellular or sub-cellular structure, metabolic processes dominate explanations of observed structure. Most entropy production is dissipated into heat loss. At more intermediate levels of organization, space, or time,
predominates. Most entropy production at this scale is dissipated into accumulating and maintaining biomass. Finally, on the largest and longest scales,
predominates, and the patterns relevant to biological explanations represent accumulation and maintenance of genetic diversity. From the perspective of the surroundings, these patterns are correlated with energy gradients, whereas from the perspective of the genealogical system, they are correlated with phylogenetic relationships and patterns of geographical distribution mirroring geological evolution occurring on similar temporal and spatial scales.
The Controversy
Theoretical studies (Prigogine and Wiame 1946) and popular texts (e.g., Schrödinger 1945; Blum 1968; Prigogine 1980) laid the groundwork for a view which, ironically, links life and its evolution to the second law mostly by its presumptive ability to circumvent the law. Schrödinger, Blum and Prigogine argued that life was physically improbable, demanding an explanation involving rare events. Following the New Synthesis, they accepted the progressive nature of evolution, also contrary to the expectations of the second law, at least in its nineteenth century formulation. Prigogine et al. developed a heuristic model in which life originated as an improbable event and evolved into increasingly improbable states. The model suggested that life could not have originated “on its own,” it must have had “outside help,” by which they meant thermodynamic flows from the surroundings into the system, deS. And they discovered something exciting—near-equilibrium, random fluctuations in the exchanges between the system and surroundings could theoretically produce states of lowered entropy. They reasoned that if such fluctuations were, on rare occasions, “captured” in a stable state, they could move themselves farther and farther away from thermodynamic equilibrium, “feeding on negentropy” (Schrödinger 1945). This view became so widespread that when Broda (1983) discussed Boltzmann’s 1905 lecture, he inserted “[negentropy]” after “entropy” throughout the text.
The metabolic duality of organisms provided presumptive support. In the process of exchanging matter and energy with their surroundings, organisms degrade their surroundings more than themselves, remaining in a low-entropy state relative to their surroundings [this is the meaning of negentropy, not that entropy has decreased]. This view informed two general concepts in biology—a form of self-organization (Depew and Weber 1995) and the principle of maximum entropy production (Swenson 1989). Superficially appearing to be the Darwinian duality (the nature of the organism and the nature of the conditions), “self-organization” in this context means the tendency for the system to organize itself according to the nature of the surroundings. The principle of maximum entropy production asserts that systems utilize resources from the surroundings as rapidly as possible, construed as a kind of selection in which whoever sequesters the most energy fastest wins, starving out their slower competitors. Both concepts ascribe causality to the surroundings; significantly absent is thermodynamic production, d
i
S. Thus, there is no “nature of the organism.”
Nor do biological systems behave as the principle of maximum entropy production suggests. Zotin and Zotina (1978) documented the general pattern. Early in ontogeny, organisms exhibit high metabolic rates, similar to maximum entropy production. This “immature” stage, however, is always replaced by a “mature” phase, characterized by reduced metabolic rate. Finally, all organisms enter a “senescent” stage in which metabolic rate decreases to a point that the organism no longer functions. This same dynamic occurs during ecosystem succession (Ulanowicz 1997). Decreasing rates of entropy production are determined by interactions between the surroundings and the “sense of self” the organism inherits from its parent(s).
In contrast with Darwin, Boltzmann felt life was a struggle for entropy, not for survival. I think both were correct. In one sense, organisms struggle to stay alive, and do so by processing matter and energy from their surroundings. They must find the necessary forms of matter and energy to sustain (their) lives. Organisms finding themselves in a place and time where such resources are available are thus able to “survive” in Boltzmann’s sense. His viewpoint is easier to see if we consider the source rather than the fate of the matter and energy organisms use to sustain life. Living systems must find usable energy. Plants find abundant “free energy” in the form of photons of light coming from the sun. The source of those photons is thermonuclear reactions in the sun involving states of matter and energy that no terrestrial life can use. Being relatively low energy products of the sun’s thermonuclear reactions “exported from the system to the surroundings,” photons are part of the sun’s entropy production. Plant biomass built using photonic energy is part of the entropy production of the plant. When an herbivore eats plant biomass, it’s feeding on entropy.
Evolution is more than just living, however, it’s descent with modification. Biological systems, from organisms to ecosystems, exist in a low-entropy state relative to their surroundings, but not relative to their own previous state. This is the result of producing and maintaining structure that is complex and organized relative to the surroundings, according to inherited information specifying internal production rules, which are largely insensitive to the details of environmental conditions (Darwin’s Necessary Misfit).