Non-biologists’ evolution

How physicists and

mathematicians try to explain
biological evolution

Ruwansha Galagedara
Origin of life
• All known organisms share the same essential features of genome
replication, gene expression, basic anabolic reactions, and
membrane-associated ATPase mediated energy production
• Monophyletic origin of all known forms of life
• Sets of genes encoding the components of above complex traits were
fixed a long time ago
• What was first? Replication or Metabolism?

Delaye, L., & Lazcano, A. (2005).

Thermodynamics of the origin of life
• Boltzmann’s struggle for “entropy”
• second law of thermodynamics
• ΔS = Q/T
• ΔS is the change in entropy, Q is the thermal energy, and T is the constant temperature
• Non-equilibrium structuring of matter in space and time – Entropy
dependent
Thermodynamics of the origin of life
• RNA and DNA are efficient absorbers of UV photons (200–300 nm )
• “dissipative structures”
• In the presence of water, extraordinarily rapid at dissipating the high
energy photons to heat
• Life arose as a catalyst for absorbing sunlight at the surface of the
shallow seas
• Promoting other irreversible abiotic processes – Eg. Water cycle
• Increase in entropy production
• UV - Inducing useful photochemical reactions and providing favorable
selective pressure
Michaelian, K. (2009)
Self-replication of DNA/RNA
• Top layer of water – most of the heat and
gas exchange between the ocean and the
atmosphere
• Accumulation of organic material at the
sea surface
Self-replication of DNA/RNA
• RNA –
• Less stable
• single strand and shorter length segments - fold in on itself or pack together
to form three dimensional structures like proteins
• catalyze chemical reactions
• But, both DNA and RNA can occur at the same time
Self-replication of DNA/RNA
• Polymerization of polynucleotide from mononucleotides - endergonic
reaction (positive free energy change)
• Will not proceed spontaneously
• Can be coupled with a second irreversible process - the absorption
and dissipation of a high energy photon
• Overall reaction is exergonic (negative free energy change)
• Early self-replication – driven by diurnal temperature variations
 • We think - the main entropic hurdle that
must be overcome by biological self-
organization as being the cost of assembling
Statistical physics of the components of the living thing in the
appropriate way
self-replication • Statistical physics –
• Calculate entropy generated in respiration
• Create a model for the probability of a
bacterium disintegrating over a set period of
time
• Heat evolved in the course of the cell
making a copy of itself is set by –
• the decrease in entropy required to arrange
molecular components of the surrounding
medium into a new organism
• how rapidly this takes place (through the
division time) and by how long we have to
wait for the newly assembled structure to
start falling apart
• Can quantify the extent of each factor’s
contribution to the final outcome
Statistical physics of self-replication
• We expect the largest contributions to the internal entropy change
for cell division to come from the equimolar conversion of oxygen to
carbon dioxide and from the confinement of amino acids floating
freely in the broth to specific locations inside bacterial proteins
• But, cost for aerobic bacterial respiration is relatively small!
• Substantially outstripped by the sheer irreversibility of the self-
replication reaction
• Statistical physics tell us that a self-replicator’s maximum potential
fitness is set by how effectively it exploits sources of energy in its
environment to catalyze its own reproduction!
Statistical physics of self-replication
• Self-replicators can increase their maximum potential growth rates by
more effectively fueling their growth via q, and by lowering the cost
of their growth and Sint.
• The less durable or the less organized a self-replicator is, all things
being equal, the less metabolic energy it must harvest at minimum in
order to achieve a certain growth rate.
• Thus, in a competition among self-replicators to dominate the
population of the future, one strategy for “success” is to be simpler in
construction and more prone to spontaneous degradation

England, J. L. (2013), England J.L. (2015)

Evolution
• Fossil record of the evolutionary history
indicated that living systems, from cells to the
biosphere, have generally increased in
complexity over time
• Empirical evidences for increase in their total
entropy production
• And net entropy production per unit biomass
• Evolution could be interpreted as a damping
response to physicochemical forces that move
a molecular system toward its most probable
state.

Davis, B. K. (1998). Krug, J. (2012).

Complexity
• Complex systems exist at different levels of organization that range
from the subatomic realm to individual organisms to whole
populations and beyond.
• With his classical book What is Life? physicist Schrödinger (1955) was
maybe the first to call attention to the problem of how the process of
life can proceed in increasing its level of complexity
• Classical Mechanisms – natural selection vs randomness

Mazzocchi, F. (2008), Ekstig, B. (2014)

Directionality in Evolution
• The Directionality Principle, which describes an increased complexity and
stability of replicating entities subject to stationary growth constraints, is a
nonequilibrium analogue of the Second Law, which describes an increase in
disorder in inanimate matter subject to irreversible processes and adiabatic
constraints.
• Directionality in populations of replicating organisms can be parametrized
in terms of a statistical concept: evolutionary entropy. (Demetrius)
• Evolutionary entropy - measure of the variability in the age of reproducing
individuals in a population, is isometric with the macroscopic variable body
size.
• Evolutionary trends in entropy due to mutation and natural selection fall
into patterns modulated by ecological and demographic constraints
Directionality in Evolution
• Demetrius’s study invokes the processes of mutation and natural
selection to provide a mechanistic explanation of macroevolutionary
trends in biopopulations
• For models of cellular populations, an analytic relation is derived
between generation time, the average length of the cell cycle, and
temperature
• show that the increase in evolutionary entropy that characterizes
population processes under density-dependent conditions represents
a nonequilibrium analogue of the second law of thermodynamics

Demetrius, L. (1997).
Modularity
• Modularity refers to the relative independence of a biological
component or network

Schuster, P., & Stadler, P. F. (2003)

Mutations
• There is compelling
evidence mutations
may not be non-
random (E. coli studies)
• Regulation of mutation
rates (non-random in
time) and localized
variation along the
genome (nonrandom
in genome space)
Goldenfeld, N., & Woese, C. (2010)
Evolutionary rate
• What determines the evolutionary rate of a population?
• Classical models of asexual populations often assume that beneficial
mutations, being rare, enter a population one at a time, i.e. they are
either lost or go to fixation before the next beneficial mutation
occurs.
• In contrast, the dynamics of multiple mutations are much more
complex—and the dependence of adaptation rate on the population
size, the mutation rate, and the selective advantage, changes
dramatically in both asexual and sexual populations
• Several physicists had tried to model evolution and adaptation using
thermodynamics and statistical physics

Kussell, E., & Vucelja, M. (2014), Perunov, N., Marsland, R. A., & England, J. L. (2016).
Evolutionary rate
• Kussel & Vucelja
• E. coli Long-term Experimental Evolution Projects
• Examine mutators and the evolution of mutation rates.
• Mutators are bacterial strains with significantly higher mutation rates than
commonly encountered in wild populations.
• In laboratory experiments, mutators have been found to evolve spontaneously,
and can become a dominant majority in a bacterial population.
• Discuss an analogy between population dynamics and polymer
thermodynamics, which identifies a key phase transition that underlies a
number of results relevant to adaptation in fluctuating environments.
• This analogy to understand the emergence of mutators as a function of
fluctuation frequency, selective strength, and mutation rates.
Statistical physics of Evolution
• Stella & Hirsch’s study
• A precise mathematical analogy can be drawn between certain
evolutionary and thermodynamic systems, allowing application of the
powerful machinery of statistical physics to analysis of a family of
evolutionary models.
• Shows that the frequencies of adaptive and deleterious substitutions at
steady state are equal.
• A free fitness function provides an analytical expression for the balance
between natural selection and stochastic drift
• Another study - Analysis of complete Archaeal and Bacterial genomes
unraveled compositional and sequence signals related to molecular
mechanisms of stability and adaptation unaffected by selective sequencing
or by the comparison of orthologs. Overall, codon bias works stronger in
Archaea and is mostly utilized in thermophilic adaptation of nucleic acids.
Stella, G. and Hirsh, A. E. (2005), Goncearenco, A., Ma, B. G., & Berezovsky, I. N. (2014).
Example: The energy–speed–accuracy trade-off in
sensory adaptation
• In biochemical networks, there are many `futile cycles', in which two
pathways run simultaneously in opposite directions dissipating
chemical energy with no apparent function.
• Here, they have showed that these cycles, are crucial in powering
accurate adaptation
• The study reveals a general relation among energy dissipation rate,
adaptation speed and the maximum adaptation accuracy

Lan, G. et al. (2012)

Quantum physics on evolution
• A target gene’s frequency depends on the proton dynamics: time
spent on different tautomers.
• If the time is short, the mutation is rare, vice versa
• Cells have the ability to do quantum measurements to drive
mutations
• Adaptive mutations occur more frequently, contradictory neo-
Darwinian theories
• Shown by Lactose tolerance in E. coli

McFadden (2002), Martin-Delgado, M. A. (2012)

Conclusions

• Evolution is less random than

we thought
• Thermodynamics, statistical
physics and quantum physics
theories have the potential be
used to explain non-equilibrium
processes we see in biological
systems
References
• Bejan, A. (2016). Life and evolution as physics. Communicative and Integrative Biology, 9(3), 1–13
• Davis, B. K. (1998). The forces driving molecular evolution. Progress in Biophysics and Molecular Biology, 69(1), 83–150
• Delaye, L., & Lazcano, A. (2005). Prebiological evolution and the physics of the origin of life. Physics of Life Reviews, 2(1), 47–64
• Demetrius, L. (1997). Directionality principles in thermodynamics and evolution. Proceedings of the National Academy of Sciences of the United
States of America, 94(8), 3491–8.
• Ekstig, B. (2014). Complexity, Natural Selection and the Evolution of Life and Humans. Foundations of Science, 20(2), 175–187
• England, J. L. (2013). Statistical physics of self-replication. Journal of Chemical Physics, 139(12).
• England, J. L. (2015). Dissipative adaptation in driven self-assembly. Nature Nanotechnology, 10(11), 919–923
• Goldenfeld, N., & Woese, C. (2010). Life is physics: evolution as a collective phenomenon far from equilibrium. Annual Review of Condensed Matter
Physics, 2, 375–399.
• Goncearenco, A., Ma, B. G., & Berezovsky, I. N. (2014). Molecular mechanisms of adaptation emerging from the physics and evolution of nucleic acids
and proteins. Nucleic Acids Research, 42(5), 2879–2892.
• Krug, J. (2012). Statistical Physics of Biological Evolution. arXiv, 2139, 1–7.
• Kussell, E., & Vucelja, M. (2014). Non-equilibrium physics and evolution—adaptation, extinction, and ecology: a Key Issues review, Reports on Progress
in Physics Rep. Prog. Phys, 77(77), 102602–15
• Lan, G., Sartori, P., Neumann, S., Sourjik, V., & Tu, Y. (2012). The energy speed accuracy trade-off in sensory adaptation. Nature Physics, 8(5), 422–428
• Martin-Delgado, M. A. (2012). On quantum effects in a theory of biological evolution. Scientific Reports, 2, 302
• Mazzocchi, F. (2008). Complexity in biology. Exceeding the limits of reductionism and determinism using complexity theory. EMBO Reports, 9(1), 10–
14.
• McFadden, J. J. (2002) Quantum Evolution: How Physics' Weirdest Theory Explains Life's Biggest Mystery, W. W. Norton & Company
• Michaelian, K. (2009). Thermodynamic Origin of Life. Earth System Dynamics, 2, 37-51
• Stella, G. and Hirsh, A. E. (2005) The application of statistical physics to evolutionary biology Pnas, 102(36), 12690–12693.
• Perunov, N., Marsland, R. A., & England, J. L. (2016). Statistical physics of adaptation. Physical Review X, 6(2), 1–12.
• Schuster, P., & Stadler, P. F. (2003). Networks in Molecular Evolution, Complexity, 8(1), 34–42.
Questions
• Do you think physics will finally give an answer to the mechanisms of
evolution?
• What do you think are the problems you found in using physics
theories to explain evolution or strengths?
• Do you think biologists should corroborate with physicists to further
clarify the processes of evolution?