On the Crucial Stages in the Origin of Animate Matter

Theories of the origin of life have proposed hypotheses to link inanimate to animate matter. The theory proposed here derived the crucial stages in the origin of animate matter directly from the basic properties of inanimate matter. It asked what were the general characteristics of the link, rather than what might have been its chemical details. Life and its origin are shown to be one continuous physicochemical process of replication, random variation, and natural selection. Since life exists here and now, animate properties must have been initiated in the past somewhere. According to the theory, life originated from an as yet unknown elementary autocatalyst which occurred spontaneously, then replicated autocatalytically. As it multiplied to macroscopic abundance, its replicas gradually exhausted their reactants. Random chemical drift initiated diversity among autocatalysts. Diversity led to competition. Competition and depletion of reactants slowed down the rates of net replication of the autocatalysts. Some reached negative rates and became extinct, while those which stayed positive ``survived.' Thus chemical natural selection appeared, the first step in the transition from inanimate to animate matter. It initiated the first animate property, fitness, i.e., the capacity to adapt to the environment and to survive. As the environment was depleted of reactants, it was enriched with sequels—namely, with decomposition products and all other products which accompany autocatalysis. The changing environment exerted a selective pressure on autocatalysts to replace dwindling reactants by accumulating sequels. Sequels that were incorporated into the autocatalytic process became internal components of complex autocatalytic systems. Primitive forms of metabolism and organization were thus initiated. They evolved further by the same mechanism to ever higher levels of complexity, such as homochirality (handedness) and membranal enclosure. Subsequent evolution by the same mechanism generated cellular metabolism, cell division, information carriers, and a genetic code. Theories of self-organization without natural selection are refuted. Received: 29 March 1996 / Accepted: 30 May 1996     

An Experimental Framework for Generating Evolvable Chemical Systems in the Laboratory

Most experimental work on the origin of life has focused on either characterizing the chemical synthesis of particular biochemicals and their precursors or on designing simple chemical systems that manifest life-like properties such as self-propagation or adaptive evolution. Here we propose a new class of experiments, analogous to artificial ecosystem selection, where we select for spontaneously forming self-propagating chemical assemblages in the lab and then seek evidence of a response to that selection as a key indicator that life-like chemical systems have arisen. Since surfaces and surface metabolism likely played an important role in the origin of life, a key experimental challenge is to find conditions that foster nucleation and spread of chemical consortia on surfaces. We propose high-throughput screening of a diverse set of conditions in order to identify combinations of “food,” energy sources, and mineral surfaces that foster the emergence of surface-associated chemical consortia that are capable of adaptive evolution. Identification of such systems would greatly advance our understanding of the emergence of self-propagating entities and the onset of adaptive evolution during the origin of life.     

From prebiotic chemistry to cellular metabolism--the chemical evolution of metabolism before Darwinian natural selection

It is generally assumed that the complex map of metabolism is a result of natural selection working at the molecular level. However, natural selection can only work on entities that have three basic features: information, metabolism and membrane. Metabolism must include the capability of producing all cellular structures, as well as energy (ATP), from external sources; information must be established on a material that allows its perpetuity, in order to safeguard the goals achieved; and membranes must be able to preserve the internal material, determining a selective exchange with external material in order to ensure that both metabolism and information can be individualized. It is not difficult to understand that protocellular entities that boast these three qualities can evolve through natural selection. The problem is rather to explain the origin of such features under conditions where natural selection could not work. In the present work we propose that these protocells could be built by chemical evolution, starting from the prebiotic primordial soup, by means of chemical selection. This consists of selective increases of the rates of certain specific reactions because of the kinetic or thermodynamic features of the process, such as stoichiometric catalysis or autocatalysis, cooperativity and others, thereby promoting their prevalence among the whole set of chemical possibilities. Our results show that all chemical processes necessary for yielding the basic materials that natural selection needs to work may be achieved through chemical selection, thus suggesting a way for life to begin.     

The origin of autonomous agents by natural selection

We propose conditions in which an autonomous agent could arise, and increase in complexity. It is assumed that on the primitive Earth there arose a recycling flow-reactor containing spontaneously formed oil droplets or lipid aggregates. These droplets grew at a basal rate by simple incorporation of lipid phase material, and divided by external agitation. This type of system was able to implement a natural selection algorithm once heredity was added. Macroevolution became possible by selection for rarely occurring chemical reactions that produced holistic autocatalytic molecular replicators (contained within the aggregate) capable of doubling at least as fast as the lipid aggregate, and which were also capable of benefiting the growth of its lipid aggregate container. No nucleotides or monomers capable of modular heredity were required at the outset. To explicitly state this hypothesis, a computer model was developed that employed an artificial chemistry, exhibiting conservation of mass and energy, incorporated within each individual of a population of lipid aggregates. This model evolved increasingly complex self-sustaining processes of constitution, a result that is also expected in real chemistry.     

ARCHAEOLOGICAL DATA REVEAL SLOW RATES OF EVOLUTION DURING PLANT DOMESTICATION

Domestication is an evolutionary process of species divergence in which morphological and physiological changes result from the cultivation/tending of plant or animal species by a mutualistic partner, most prominently humans. Darwin used domestication as an analogy to evolution by natural selection although there is strong debate on whether this process of species evolution by human association is an appropriate model for evolutionary study. There is a presumption that selection under domestication is strong and most models assume rapid evolution of cultivated species. Using archaeological data for 11 species from 60 archaeological sites, we measure rates of evolution in two plant domestication traits—nonshattering and grain/seed size increase. Contrary to previous assumptions, we find the rates of phenotypic evolution during domestication are slow, and significantly lower or comparable to those observed among wild species subjected to natural selection. Our study indicates that the magnitudes of the rates of evolution during the domestication process, including the strength of selection, may be similar to those measured for wild species. This suggests that domestication may be driven by unconscious selection pressures similar to that observed for natural selection, and the study of the domestication process may indeed prove to be a valid model for the study of evolutionary change.     

The uniqueness of biological self-organization: challenging the Darwinian paradigm

Here we discuss the challenge posed by self-organization to the Darwinian conception of evolution. As we point out, natural selection can only be the major creative agency in evolution if all or most of the adaptive complexity manifest in living organisms is built up over many generations by the cumulative selection of naturally occurring small, random mutations or variants, i.e., additive, incremental steps over an extended period of time. Biological self-organization—witnessed classically in the folding of a protein, or in the formation of the cell membrane—is a fundamentally different means of generating complexity. We agree that self-organizing systems may be fine-tuned by selection and that self-organization may be therefore considered a complementary mechanism to natural selection as a causal agency in the evolution of life. But we argue that if self-organization proves to be a common mechanism for the generation of adaptive order from the molecular to the organismic level, then this will greatly undermine the Darwinian claim that natural selection is the major creative agency in evolution. We also point out that although complex self-organizing systems are easy to create in the electronic realm of cellular automata, to date translating in silico simulations into real material structures that self-organize into complex forms from local interactions between their constituents has not proved easy. This suggests that self-organizing systems analogous to those utilized by biological systems are at least rare and may indeed represent, as pre-Darwinists believed, a unique ascending hierarchy of natural forms. Such a unique adaptive hierarchy would pose another major challenge to the current Darwinian view of evolution, as it would mean the basic forms of life are necessary features of the order of nature and that the major pathways of evolution are determined by physical law, or more specifically by the self-organizing properties of biomatter, rather than natural selection.     

Beauty or function? The opposing effects of natural and sexual selection on cuticular hydrocarbons in male black field crickets

Although many theoretical models of male sexual trait evolution assume that sexual selection is countered by natural selection, direct empirical tests of this assumption are relatively uncommon. Cuticular hydrocarbons (CHCs) are known to play an important role not only in restricting evaporative water loss but also in sexual signalling in most terrestrial arthropods. Insects adjusting their CHC layer for optimal desiccation resistance is often thought to come at the expense of successful sexual attraction, suggesting that natural and sexual selection are in opposition for this trait. In this study, we sampled the CHCs of male black field crickets (Teleogryllus commodus) using solid-phase microextraction and then either measured their evaporative water loss or mating success. We then used multivariate selection analysis to quantify the strength and form of natural and sexual selection targeting male CHCs. Both natural and sexual selection imposed significant linear and stabilizing selection on male CHCs, although for very different combinations. Natural selection largely favoured an increase in the total abundance of CHCs, especially those with a longer chain length. In contrast, mating success peaked at a lower total abundance of CHCs and declined as CHC abundance increased. However, mating success did improve with an increase in a number of specific CHC components that also increased evaporative water loss. Importantly, this resulted in the combination of male CHCs favoured by natural selection and sexual selection being strongly opposing. Our findings suggest that the balance between natural and sexual selection is likely to play an important role in the evolution of male CHCs in T. commodus and may help explain why CHCs are so divergent across populations and species.     

Impact of selection on genes involved in regulatory network: a modelling study

Complex phenotypes are often controlled by many interacting genes. One question emerging from such organization is how selection, acting at the phenotypic level, shapes the evolution of genes involved in regulatory networks controlling the phenotypes. We studied this issue through a matrix model of such networks. In a population submitted to selection, we simulated the evolution of a quantitative trait controlled by a set of loci that regulate each other through positive or negative interactions. Investigating several levels of selection intensity on the trait, we studied the evolution of regulation intensity between the genes and the evolution of the genetic diversity of those genes as an indirect measure of the strength of selection acting on them. We show that an increasing intensity of selection on the phenotype leads to an increased level of regulation between the loci. Moreover, we found that the genes responding more strongly to selection within the network were those evolving towards stronger regulatory action on the other genes and/or those that are the less regulated by the other genes. This observation is strongest for an intermediate level of selection. This may explain why several experimental studies have shown evidence of selection on regulatory genes inside gene networks.     

Detecting individual sites subject to episodic diversifying selection

The imprint of natural selection on protein coding genes is often difficult to identify because selection is frequently transient or episodic, i.e. it affects only a subset of lineages. Existing computational techniques, which are designed to identify sites subject to pervasive selection, may fail to recognize sites where selection is episodic: a large proportion of positively selected sites. We present a mixed effects model of evolution (MEME) that is capable of identifying instances of both episodic and pervasive positive selection at the level of an individual site. Using empirical and simulated data, we demonstrate the superior performance of MEME over older models under a broad range of scenarios. We find that episodic selection is widespread and conclude that the number of sites experiencing positive selection may have been vastly underestimated.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae)

Closely related animal lineages often vary in male coloration, and ecological selection is hypothesized to shape this variation. The role of ecological selection in inhibiting male color has been documented extensively at the population level, but relatively few studies have investigated the evolution of male coloration across a clade of closely related species. Darters are a diverse group of fishes that vary in the presence of elaborate male nuptial coloration, with some species exhibiting vivid color patterns and others mostly or entirely achromatic. We used phylogenetic logistic regression to test for correlations between the presence/absence of color traits across darter species and the ecological conditions in which these species occur. Environmental variables were correlated with the presence of nuptial color in darters with colorful species tending to inhabit environments that would support fewer predators and potentially transmit a broader spectrum of natural light compared to species lacking male coloration. We also tested the color preferences of a common darter predator, largemouth bass, and found that it exhibits a strong preference for red, providing further evidence of predation as a source of selection on color evolution in darters. Ecological selection therefore appears to be an important factor in dictating the presence or absence of male coloration in this group of fishes.     

The consequences of phenotypic plasticity for ecological speciation

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.     

Cultural niche construction and human evolution

Organisms frequently choose, regulate, construct and destroy important components of their environments, in the process changing the selection pressures to which they and other organisms are exposed. We refer to these processes as niche construction. In humans, culture has greatly amplified our capacity for niche construction and our ability to modify selection pressures. We use gene‐culture coevolutionary models to explore the evolutionary consequences of culturally generated niche construction through human evolution. Our analysis suggests that where cultural traits are transmitted in an unbiased fashion from parent to offspring, cultural niche construction will have a similar effect to gene‐based niche construction. However, cultural transmission biases favouring particular cultural traits may either increase or reduce the range of parameter space over which niche construction has an impact, which means that niche construction with biased transmission will either have a much smaller or a much bigger effect than gene‐based niche construction. The analysis also reveals circumstances under which cultural transmission can overwhelm natural selection, accelerate the rate at which a favoured gene spreads, initiate novel evolutionary events and trigger hominid speciation. Because cultural processes typically operate faster than natural selection, cultural niche construction probably has more profound consequences than gene‐based niche construction, and is likely to have played an important role in human evolution.     

Critical-like self-organization and natural selection: Two facets of a single evolutionary process?

We argue that critical-like dynamics self-organize relatively easily in non-equilibrium systems, and that in biological systems such dynamics serve as templates upon which natural selection builds further elaborations. These critical-like states can be modified by natural selection in two fundamental ways, reflecting the selective advantage (if any) of heritable variations either among avalanche participants or among whole systems. First, reproducing (avalanching) units can differentiate, as units adopt systematic behavioural variations. Second, whole systems that are exposed to natural selection can become increasingly or decreasingly critical. We suggest that these interactions between SOC-like dynamics and natural selection have profound consequences for biological systems because they could have facilitated the evolution of division of labour, compartmentalization and computation, key features of biological systems. The logical conclusion of these ideas is that the fractal geometry of nature is anything but coincidental, and that natural selection is itself a fractal process, occurring on many temporal and spatial scales.     

Pollinators exert positive selection on flower size on urban,but not on rural Scotch broom (Cytisus scoparius L. Link)

Aims Adaptive evolution of invasive species is both particularly exciting for the evolutionary biologist and worrisome for those interested in controlling or halting spread. Invasive species often have a distinct timeline and well-recorded population expansion. As invaders encounter new environments, they undergo rapid adaptive evolution. Our aim in this study was to measure variation of floral size in the invasive shrub Cytisus scoparius (Scotch broom) and measure natural selection by pollinators on that trait. Past research has found that this invasive plant is pollinator limited in Washington State and that declines in pollinator populations can contribute to local extinction in another invaded range (New Zealand). This plant is pollinated by both native and introduced species of bees, representing a broad range of pollinator sizes. Cytisus scoparius has a flower structure that is highly conducive to studies on pollinator choice, even in the absence of direct pollinator observations.Methods We surveyed urban and rural sites in and around the city of Olympia in Washington State. Measuring banner width, we were able to show that flower size varies substantially between plants but minimally within plants. By measuring the proportion of flowers that were 'tripped', we could determine pollinator visitation rates and thus determine the level of selection due to pollinator choice alone.Important findings We found that C. scoparius is under natural selection by pollinators for increased flower size. However, such positive natural selection was only seen in urban populations although it was consistent across two flowering seasons. Rural populations of Scotch broom do not appear to be under selection on flower size. The natural selection by pollinators on broom flowers could result in adaptive evolution into a new pollination niche by an invading species. A higher level of variation in broom flowers seen here than seen in previous works in native regions suggests that C. scoparius may be highly diverse and primed for adaptive evolution.     

The evolution and evolutionary consequences of marginal thermostability in proteins

When we seek to explain the characteristics of living systems in their evolutionary context, we are often interested in understanding how and why certain properties arose through evolution, and how these properties then affected the continuing evolutionary process. This endeavor has been assisted by the use of simple computational models that have properties characteristic of natural living systems but allow simulations over evolutionary timescales with full transparency. We examine a model of the evolution of a gene under selective pressure to code for a protein that exists in a prespecified folded state at a given growth temperature. We observe the emergence of proteins with modest stabilities far below those possible with the model, with a denaturation temperature tracking the simulation temperature, despite the absence of selective pressure for such marginal stability. This demonstrates that neither observations of marginally stable proteins, nor even instances where increased stability interferes with function, provide evidence that marginal stability is an adaptation. Instead the marginal stability is the result of a balance between predominantly destabilizing mutations and selection that shifts depending on effective population size. Even if marginal stability is not an adaptation, the natural tendency of proteins toward marginal stability, and the range of stabilities that occur during evolution, may have significant effect on the evolutionary process.     

Global phylogeny determined by the combination of protein domains in proteomes

The majority of proteins consist of multiple domains that are either repeated or combined in defined order. In this study, we survey the combination of protein domains defined at fold and fold superfamily levels in 185 genomes belonging to organisms that have been fully sequenced and introduce a method that reconstructs rooted phylogenomic trees from the content and arrangement of domains in proteins at a genomic level. We find that the majority of domain combinations were unique to Archaea, Bacteria, or Eukarya, suggesting most combinations originated after life had diversified. Domain repeat and domain repeat within multidomain proteins increased notably in eukaryotes, mainly at the expense of single-domain and domain-pair proteins. This increase was mostly confined to Metazoa. We also find an unbalanced sharing of domain combinations which suggests that Eukarya is more closely related to Bacteria than to Archaea, an observation that challenges the widely assumed eukaryote-archaebacterial sisterhood relationship. The occurrence and abundance of the molecular repertoire (interactome) of domain combinations was used to generate phylogenomic trees. These global interactome-based phylogenies described organismal histories satisfactorily, revealing the tripartite nature of life, and supporting controversial evolutionary patterns, such as the Coelomata hypothesis, the grouping of plants and animals, and the Gram-positive origin of bacteria. Results suggest strongly that the process of domain combination is not random but curved by evolution, rejecting the null hypothesis of domain modules combining in the absence of natural selection or an optimality criterion.     

Modeling microbial consortiums as distributed metabolic networks

Biogeochemistry is the study of how living systems in combination with abiotic reactions process and cycle mass and energy on local, regional, and global scales (Schlesinger, 1997). Understanding how these biogeochemical cycles function and respond to perturbations has become increasingly important, as anthropogenic impacts have significantly altered many of these cycles (Galloway and Cowling, 2002; Houghton et al., 2002). Biogeochemistry is strongly governed by microbial processes, and it appears to closely follow thermodynamic constraints in that electron acceptor (O(2), NO(3)(-), SO(4)(2-), etc.) utilization closely follows a priori expectations based on energetics (Vallino et al., 1996; Hoehler et al., 1998; Jakobsen and Postma, 1999; Amend and Shock, 2001). Consortiums of microorganisms seem to have evolved to exploit chemical potentials wherever they exist in the environment, as manifested by the recent discovery of anaerobic methane oxidation by sulfate (Boetius et al., 2000) or sulfide oxidation by nitrate (Schulz et al., 1999). Three and a half billion years of natural selection have produced living systems capable of degrading most chemical potentials. We may therefore ask: If all ecosystem niche space is filled, is the biogeochemistry we observe in the environment dependent on the organisms that occupy that environment, or is the biogeochemistry determined by fundamental forces, with the evolution of living systems being the implementation of those forces? Recent developments in nonequilibrium thermodynamics (NET) are beginning to support the latter alternative, and advances in genomics are allowing us to explore microbial consortiums in detail. Taking advantage of ideas being suggested by NET, we have developed a modeling framework that views microbial consortiums as an inter-species distributed metabolic network. When combined with experimental observations, the model should help us test hypotheses that govern how living systems function.     

Food choice by white-tailed deer in relation to protein and energy content of the diet: a field experiment

Optimality models of food selection by herbivores assume that individuals are capable of assessing forage value, either directly through the currency used in the model or indirectly through other variables correlated with the currency. Although energy and protein are the two currencies most often used, controversy exists regarding their respective influence on food choice. Part of the debate is due to the difficulty of teasing apart these two nutrients, which are closely correlated in most natural forages. Here we offer a test of the assumption that energy and protein contents of the forage are both currencies that large mammalian herbivores can use when selecting their food. We observed feeding behavior of 47 wild white-tailed deer (Odocoileusvirginianus) during winter while individuals were presented with four experimental foods representing two levels of energy and protein (dry matter digestibility: 40–50%; crude protein: 12–16%). Using experimental foods allowed us to separate the influences of energy and protein and clearly distinguish between the roles of these two nutrients. Deer discriminated between foods through partial selection, and selected diets higher in energy but lower in protein. The observed choices appeared consistent with physiological needs of deer wintering at the study site, where digestible energy was in short supply in the natural environment while protein was probably not. Results are in good agreement with recent findings on domesticated ruminants. They support a basic assumption of optimality models of food selection that use energy and/or protein as a currency, although the physiological mechanisms behind the food selection process remain unclear. We urge students of food selection by herbivores to replicate our experiment with other foods and/or in other circumstances before more general conclusions are drawn. Received: 1 September 1997 / Accepted: 22 February 1998     

Inevitable evolution: back to the origin and beyond the 20th century paradigm of contingent evolution by historical natural selection

Since neo-Darwinism arose from the work of Darwin and Mendel evolution by natural selection has been seen as contingent and historical being defined by an a posteriori selection process with no a priori laws that explain why evolution on Earth has taken the direction of the major evolutionary trends and transitions instead of any other direction. Recently, however, major life-history trends and transitions have been explained as inevitable because of a deterministic selection that unfolds from the energetic state of the organism and the density-dependent competitive interactions that arise from self-replication in limited environments. I describe differences and similarities between the historical and deterministic selection processes, illustrate concepts using life-history models on large body masses and limited reproductive rates, review life-history evolution with a wider focus on major evolutionary transitions, and propose that biotic evolution is driven by a universal natural selection where the long-term evolution of fitness-related traits is determined mainly by deterministic selection, while contingency is important predominately for neutral traits. Given suitable environmental conditions, it is shown that selection by energetic state and density-dependent competitive interactions unfolds to higher level selection for life-history transitions from simple asexually reproducing self-replicators to large bodied organisms with senescence and sexual reproduction between males and females, and in some cases, to the fully evolved eusocial colony with thousands of offspring workers. This defines an evolutionary arrow of time for open thermodynamic systems with a constant inflow of energy, predicting similar routes for long-term evolution on similar planets.