Susanna C. Manrubia

Criticality and scaling in evolutionary ecology.

Fluctuations in ecological systems are known to involve a wide range of spatial and temporal scales, often displaying self-similar (fractal) properties. Recent theoretical approaches are trying to shed light on the nature of these complex dynamics. The results suggest that complexity in ecology and evolution comes from the network-like structure of multispecies communities that are close to instability. If true, these ideas might change our understanding of how complexity emerges in the biosphere and how macroevolutionary events could be decoupled from microevolutionary ones.

Self-similarity of extinction statistics in the fossil record

The dynamical processes underlying evolution over geological timescales remain unclear,. Analyses of time series of the fossil record have highlighted the possible signature of periodicity in mass extinctions,, perhaps owing to external influences such as meteorite impacts. More recently the fluctuations in the evolutionary record have been proposed to result from intrinsic nonlinear dynamics for which self-organized criticality provides an appropriate theoretical framework. A consequence of this controversial conjecture is that the fluctuations should be self-similar, exhibiting scaling behaviour like that seen in other biological and socioeconomic, systems. The self-similar character is described by a 1/f power spectrum P(f), which measures the contributions of each frequency f to the overall time series. If self-similarity is present, then P(f) ≈ f − β with 0 < β <2. This idea has not been sufficiently tested, however, owing to a lack of adequate data. Here we explore the statistical fluctuation structure of several time series obtained from available palaeontological data bases, particularly the new ‘Fossil Record 2’. We find that these data indeed show self-similar fluctuations characterized by a 1/f spectrum. These findings support the idea that a nonlinear response of the biosphere to perturbations provides the main mechanism for the distribution of extinction events.

Evolutionary Transition toward Defective RNAs That Are Infectious by Complementation

ABSTRACT Passage of foot-and-mouth disease virus (FMDV) in cell culture resulted in the generation of defective RNAs that were infectious by complementation. Deletions (of nucleotides 417, 999, and 1017) mapped in the L proteinase and capsid protein-coding regions. Cell killing followed two-hit kinetics, defective genomes were encapsidated into separate viral particles, and individual viral plaques contained defective genomes with no detectable standard FMDV RNA. Infection in the absence of standard FMDV RNA was achieved by cotransfection of susceptible cells with transcripts produced in vitro from plasmids encoding the defective genomes. These results document the first step of an evolutionary transition toward genome segmentation of an unsegmented RNA virus and provide an experimental system to compare rates of RNA progeny production and resistance to enhanced mutagenesis of a segmented genome versus its unsegmented counterpart.

Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss.

RNA viruses display high mutation rates and their populations replicate as dynamic and complex mutant distributions, termed viral quasispecies. Repeated genetic bottlenecks, which experimentally are carried out through serial plaque-to-plaque transfers of the virus, lead to fitness decrease (measured here as diminished capacity to produce infectious progeny). Here we report an analysis of fitness evolution of several low fitness foot-and-mouth disease virus clones subjected to 50 plaque-to-plaque transfers. Unexpectedly, fitness decrease, rather than being continuous and monotonic, displayed a fluctuating pattern, which was influenced by both the virus and the state of the host cell as shown by effects of recent cell passage history. The amplitude of the fluctuations increased as fitness decreased, resulting in a remarkable resistance of virus to extinction. Whereas the frequency distribution of fitness in control (independent) experiments follows a log-normal distribution, the probability of fitness values in the evolving bottlenecked populations fitted a Weibull distribution. We suggest that multiple functions of viral genomic RNA and its encoded proteins, subjected to high mutational pressure, interact with cellular components to produce this nontrivial, fluctuating pattern.

Eukaryotic community distribution and its relationship to water physicochemical parameters in an extreme acidic environment, Rio Tinto (southwestern Spain).

ABSTRACT The correlation between water physicochemical parameters and eukaryotic benthic composition was examined in Río Tinto. Principal component analysis showed a high inverse relationship between pH and most of the heavy metals analyzed as well as Dunaliella sp., while Chlamydomonas sp. abundance was positively related. Zn, Cu, and Ni clustered together and showed a strong inverse correlation with the diversity coefficient and most of the species analyzed. These eukaryotic communities seem to be more influenced by the presence of heavy metals than by the pH.

Mutual synchronization and clustering in randomly coupled chaotic dynamical networks

We introduce and study systems of randomly coupled maps where the relevant parameter is the degree of connectivity in the system. Global (almost-) synchronized states are found (equivalent to the synchronization observed in globally coupled maps) until a certain critical threshold for the connectivity is reached. We further show that not only the average connectivity, but also the architecture of the couplings is responsible for the cluster structure observed. We analyze the different phases of the system and use various correlation measures in order to detect ordered nonsynchronized states. Finally, it is shown that the system displays a dynamical hierarchical clustering which allows the definition of emerging graphs.

Vertical transmission of culture and the distribution of family names

A stochastic model for the evolution of a growing population is proposed, in order to explain empirical power-law distributions in the frequency of family names as a function of the family size. Preliminary results show that the predicted exponents are in good agreement with real data. The evolution of family-name distributions is discussed in the frame of vertical transmission of cultural features.

Population Bottlenecks in Quasispecies Dynamics

The characteristics of natural populations result from different stochastic and deterministic processes that include reproduction with error, selection, and genetic drift. In particular, population fluctuations constitute a stochastic process that may play a very relevant role in shaping the structure of populations. For example, it is expected that small asexual populations will accumulate mutations at a higher rate than larger ones. As a consequence, in any population the fixation of mutations is accelerated when environmental conditions cause population bottlenecks. Bottlenecks have been relatively frequent in the history of life and it is generally accepted that they are highly relevant for speciation. Although population bottlenecks can occur in any species, their effects are more noticeable in organisms that form large and heterogeneous populations, such as RNA viral quasispecies. Bottlenecks can also positively select and isolate particles that still keep the ability to infect cells from a disorganized population created by crossing the error threshold.

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.

Potential Benefits of Sequential Inhibitor-Mutagen Treatments of RNA Virus Infections

Lethal mutagenesis is an antiviral strategy consisting of virus extinction associated with enhanced mutagenesis. The use of non-mutagenic antiviral inhibitors has faced the problem of selection of inhibitor-resistant virus mutants. Quasispecies dynamics predicts, and clinical results have confirmed, that combination therapy has an advantage over monotherapy to delay or prevent selection of inhibitor-escape mutants. Using ribavirin-mediated mutagenesis of foot-and-mouth disease virus (FMDV), here we show that, contrary to expectations, sequential administration of the antiviral inhibitor guanidine (GU) first, followed by ribavirin, is more effective than combination therapy with the two drugs, or than either drug used individually. Coelectroporation experiments suggest that limited inhibition of replication of interfering mutants by GU may contribute to the benefits of the sequential treatment. In lethal mutagenesis, a sequential inhibitor-mutagen treatment can be more effective than the corresponding combination treatment to drive a virus towards extinction. Such an advantage is also supported by a theoretical model for the evolution of a viral population under the action of increased mutagenesis in the presence of an inhibitor of viral replication. The model suggests that benefits of the sequential treatment are due to the involvement of a mutagenic agent, and to competition for susceptible cells exerted by the mutant spectrum. The results may impact lethal mutagenesis-based protocols, as well as current antiviral therapies involving ribavirin.