David A. Baum

A key criticism of metabolism-first theories of abiogenesis is that, in the absence of specialized catalysts, side reactions would convert too many autocatalysts to inert by-products for autocatalytic systems to persist. Here, we use algebraic analysis and numerical simulations to explore the effects of side reactions on the persistence of simple autocatalytic systems. For an autocatalytic reaction coupled to a side reaction, whenever a component reaction is strictly irreversible, which is technically impossible but frequently considered an acceptable approximation, side reactions harm autocatalytic systems. But if all reactions are assumed reversible, perhaps with unequal forward and reverse rate constants, side reactions can have a wide range of effects—they can be harmful, neutral, beneficial, or harmful in the short term but beneficial in the longer term. These effects arise in the presence of reversible reactions, because side products can also serve as a reservoir from which autocatalysts can be re-derived. We then use algebraic analysis to confirm that such diverse effects also apply to a larger autocatalytic cycle coupled to more side reactions. Our results show that the effects of side reactions on autocatalytic systems do not provide sufficient grounds to reject metabolism-first models.

Biological individuals on Earth today are cellular, but the simplest cells are too complex to have arisen spontaneously. We explore the hypothesis that the emergence of biological individuality might have been driven by selection for different molecules to move through space together by forming a propagule. We predicted that propagule formation will be advantageous to an autocatalytic system primarily when 1) sites supporting autocatalysis are distantly spaced and 2) the environment undergoes periodic disturbances. We tested this hypothesis using computational reaction-diffusion models of surface-catalyzed autocatalytic systems in patchy, disturbance-prone environments. We considered two competing autocatalytic cycles, each composed of mutualistic subcycles, one of which diverts flux to the production of propagules. Our analysis shows that propagules tend to be detrimental in well-mixed environments or environments where viable surfaces are close enough together to be reliably seeded through single-species dispersal. However, propagule formation is advantageous when long stretches of empty space must be crossed to reach new resources and/or when environmental disturbances are frequent. These findings suggest spatial structure can selectively favor reliable forms of codispersal. Evolution in response to this mechanism could potentially explain the emergence of vesicles that transported many autocatalytic species and eventually became independent protocells.

Baobab trees ( Adansonia ) are iconic members of Madagascar's biota that serve as emblems for the island's unique biodiversity. Despite this recognition, many questions remain regarding evolutionary relationships and species limits within the genus. We used custom‐designed targeted sequence capture data to obtain phased allelic sequences for hundreds of nuclear loci and plastomes. Using broad geographic sampling, representing all species in the genus, and including a few possible hybrid individuals, we reconstructed the population history of Malagasy baobabs using network inference methods to detect reticulation. We obtained a species tree that is well supported, but with clear cases of reticulation, most notably admixture between Adansonia rubrostipa and A. madagascariensis in northwestern Madagascar, and instances of introgression involving the widespread species, A. za . Analysis of exclusivity factors suggests elevating one variety of A. za to the species rank, and also raises the possibility, pending additional sampling, of splitting A. rubrostipa into two species. We discuss the implications of gene flow on species delimitation and diversification in the context of conservation efforts for these iconic and threatened trees. Given our results, we formally resurrect the species A. bozy from A. za var. bozy , thus raising the number of endemic Malagasy baobab species from six to seven.

Adaptive evolution has long been hypothesized to be possible in the absence of genetic molecules, but experimental evidence remains lacking. Fatty acid vesicles can spontaneously grow and divide and might therefore be capable of nongenetic inheritance, making them ideal for exploring the emergence of prebiotic evolution. In this study, we tested whether vesicle populations can respond to artificial selection for greater turbidity and, if so, whether that response can be tied to an inheritance-like mechanism. We prepared 192 independent vesicle populations, incubated them for 24 h, and then selected half of the populations to propagate into the next generation. The populations to propagate were picked either randomly, representing drift controls, or were those with the greatest turbidity, representing selection. Population propagation involved resuspension, transfer into fresh buffer, feeding with an amphiphile stock, and then incubating for the next 24 h. In three replicate experiments run for at least 10 generations, we observed consistently greater turbidity in selection compared with drift lineages. This was accompanied by a reduction in the heritability (the regression slope between parent and offspring turbidities) of the selected lineages. We conducted additional experiments to evaluate whether this response to selection is caused by a simple carryover effect or reflects cooperative dynamics where vesicles from a parental population affect newly formed vesicles in the next generation. The response to selection is much lower when the resuspension step was omitted and/or if new amphiphiles were provided as preformed vesicles. Combined with fluorescence analyses of the resuspension and feeding processes, these results suggest that cooperative vesicle dynamics occur in cases where a small number of intact vesicles from a parental generation interact with an excess of incorporated amphiphiles. Overall, this study represents the first experimental finding of a response to artificial selection in prebiotic chemistry.

In origins-of-life research, a key challenge is to explain the emergence of polymers of sufficient length to confer the complex functions needed for genetic inheritance. Previous studies have demonstrated that prebiotic environments enabling multilevel selection can facilitate the survival of cooperating polymers such as ribozymes, which allows that complex functions undertaken today by long polymers might have originated from multiple simpler functions undertaken by shorter polymers. To further investigate this possibility, we developed a new computational model of cooperative catalytic and replicating polymer systems that avoids tracking all possible polymer sequences. This approach scales well computationally, avoiding the need to set an a priori cap on polymer length. We first validated this model by replicating key conclusions of previous studies, for example that the persistence of cooperative synthetase-ligase systems is facilitated by both intrinsic factors (shorter length, higher catalytic efficiency) and by factors that promote multilevel-selection (compartmentalization, slower diffusion). We then explored the effects of introducing a mutation inhibitor into a cooperative synthetase-ligase system. The results support the possibility that mutation inhibition could have arisen, not through the appearance of a single proofreading polymerase, but through the emergence of distinct, mutation inhibiting catalysts.

Adaptive evolution has long been hypothesized to be possible in the absence of genetic molecules, but experimental evidence remains lacking. Fatty acid vesicles represent an intriguing model to study the emergence of prebiotic evolution, since they can spontaneously grow and divide and have been hypothesized to be capable of non-genetic inheritance. In this study we conducted multiple experiments to test whether vesicle populations can respond to artificial selection for greater turbidity and, if so, whether that response can be tied to an inheritance-like mechanism. We prepared 96 independent vesicle populations, incubated them for 24 hours and then selected half the populations to propagate into the next generation. The populations to propagate were picked either randomly ,representing drift controls, or were the populations with the greatest turbidity, representing selection. Population propagation involved resuspension, transfer into fresh buffer, feeding with an amphiphile stock, and then incubating for the next 24 hours. In three replicate experiments run for at least 10 generations, we observed consistently greater turbidity in selection lineages compared to drift, as well as a reduction in the heritability (i.e., the correlation between parent and offspring turbidities). We conducted additional experiments to evaluate whether this response to selection is caused by a simple carryover effect or reflects cooperative dynamics, where vesicles from the parental generation affect newly formed vesicles in the offspring generation. The response to selection is much lower if we omitted the resuspension step and/or if we did not feed transfers with amphiphiles but instead mixed them we pre-formed vesicles. Combined with imaging and other analyses of the resuspension and feeding process, these results suggest that cooperative vesicle dynamics occur, where a small number of intact vesicles from a parental generation alters the dynamics of new vesicle formation following food addition. Overall, this study represents the first experimental finding of a response to artificial selection in prebiotic chemistry.

A key criticism of metabolism-first theories of abiogenesis is that, in the absence of specialized catalysts, side reactions would convert too many autocatalysts to inert byproducts for autocatalytic systems to persist. Here we use algebraic analysis and numerical simulations to explore the effects of side reactions on the persistence of simple autocatalytic systems. For an autocatalytic reaction coupled to a side reaction, whenever a component reaction is strictly irreversible, which is technically impossible but frequently considered an acceptable approximation, side reactions harm autocatalytic systems. But if all reactions are assumed reversible, perhaps with unequal forward and reverse rate constants, side reactions can have a wide range of effects – they can be harmful, neutral, beneficial, or harmful in the short term but beneficial in the longer term. These effects arise in the presence of reversible reactions, because side products can also serve as a reservoir from which autocatalysts can be re-derived. We then use algebraic analysis to confirm that such diverse effects also apply to a larger autocatalytic cycle coupled to more side reactions. Our results show that the effects of side reactions on autocatalytic systems do not provide sufficient grounds to reject metabolism-first models.

Autocatalysis is thought to have played an important role in the earliest stages of the origin of life. An autocatalytic cycle (AC) is a set of reactions that results in stoichiometric increase in its constituent chemicals. When the reactions of multiple interacting ACs are active in a region of space, they can have interactions analogous to those between species in biological ecosystems. Prior studies of autocatalytic chemical ecosystems (ACEs) have suggested avenues for accumulating complexity, such as ecological succession, as well as obstacles such as competitive exclusion. We extend this ecological framework to investigate the effects of surface adsorption, desorption, and diffusion on ACE ecology. Simulating ACEs as particle-based stochastic reaction-diffusion systems in spatial environments—including open, two-dimensional reaction-diffusion systems and adsorptive mineral surfaces—we demonstrate that spatial structure can enhance ACE diversity by (i) permitting otherwise mutually exclusive ACs to coexist and (ii) subjecting new AC traits to selection.

Explaining the origin of molecular systems composed of cooperating polymer sets that confer both metabolic and information processing functions is a key challenge in origins-of-life research. A related puzzle is the emergence of polymers of sufficient length to confer complex functions such as the RNA-dependent RNA polymerization with proofreading. Addressing these issues using computational models of template-guided replicating polymer systems is generally constrained by the exponential increase in diversity as the length of polymers increases. In this study, inspired by the computer game Tetris® and the P olymerase C hain R eaction (PCR) technique, we developed an abstract computational model of cooperative replicating polymer systems that avoids tracking all potential sequences. Using this model, we explored cooperative chemical ecosystems consisting of catalytic polymers conferring functions analogous to kinases, ligases, and mutation inhibitors. We show that prebiotic environments with micro-compartments with local exchanges enable multilevel selection that facilitates the survival of cooperating polymers. The ability of cooperative systems to persist is sensitive to intrinsic properties of catalysts such as catalytic efficiency and extrinsic factors such as dilution rate. These results provide a roadmap for future studies that look not just at persistence but also at the stepwise, de novo emergence of chemical ecosystems with both metabolic and information-processing capabilities.

While modern physics and biology satisfactorily explain the passage from the Big Bang to the formation of Earth and the first cells to present-day life, respectively, the origins of biochemical life still remain an open question. Since life, as we know it, requires extremely long genetic polymers, any answer to the question must explain how an evolving system of polymers of ever-increasing length could come about on a planet that otherwise consisted only of small molecular building blocks. In this work we show that, under realistic constraints, an abstract polymer model can exhibit dynamics such that attractors in the polymer population space with a higher average polymer length are also more probable. We generalize from the model and formalize the notions of and for chemical reaction networks with multiple attractors. The complexity of a species is defined as the minimum number of reactions needed to produce it from a set of building blocks, which in turn is used to define a measure of complexity for an attractor. A transition between attractors is considered to be a if the attractor with the higher probability also has a higher complexity. In an environment where only monomers are readily available, the attractor with a higher average polymer length is more complex. Thus, by this criterion, our abstract polymer model can exhibit progressive evolution for a range of thermodynamically plausible rate constants. We also formalize criteria for and evolution and explain the role of autocatalysis in obtaining them. Our work provides a basis for searching for prebiotically plausible scenarios in which long polymers can emerge and yield populations with even longer polymers. Additionally, the existence of features like history dependence and open endedness support the view that the path from chemistry to biology was one of gradual complexification rather than an instantaneous origin of life. Published by the American Physical Society 2025