Unity and disunity in evolutionary sciences: Process-based analogies open common research avenues for biology and linguistics

International audienceBackgroundFor a long time biologists and linguists have been noticing surprising similarities between the evolution of life forms and languages. Most of the proposed analogies have been rejected. Some, however, have persisted, and some even turned out to be fruitful, inspiring the transfer of methods and models between biology and linguistics up to today. Most proposed analogies were based on a comparison of the research objects rather than the processes that shaped their evolution. Focusing on process-based analogies, however, has the advantage of minimizing the risk of overstating similarities, while at the same time reflecting the common strategy to use processes to explain the evolution of complexity in both fields.ResultsWe compared important evolutionary processes in biology and linguistics and identified processes specific to only one of the two disciplines as well as processes which seem to be analogous, potentially reflecting core evolutionary processes. These new process-based analogies support novel methodological transfer, expanding the application range of biological methods to the field of historical linguistics. We illustrate this by showing (i) how methods dealing with incomplete lineage sorting offer an introgression-free framework to analyze highly mosaic word distributions across languages; (ii) how sequence similarity networks can be used to identify composite and borrowed words across different languages; (iii) how research on partial homology can inspire new methods and models in both fields; and (iv) how constructive neutral evolution provides an original framework for analyzing convergent evolution in languages resulting from common descent (Sapir’s drift).ConclusionsApart from new analogies between evolutionary processes, we also identified processes which are specific to either biology or linguistics. This shows that general evolution cannot be studied from within one discipline alone. In order to get a full picture of evolution, biologists and linguists need to complement their studies, trying to identify cross-disciplinary and discipline-specific evolutionary processes. The fact that we found many process-based analogies favoring transfer from biology to linguistics further shows that certain biological methods and models have a broader scope than previously recognized. This opens fruitful paths for collaboration between the two disciplines

Reconstructing phylogenetic level-1 networks from nondense binet and trinet sets

Binets and trinets are phylogenetic networks with two and three leaves, respectively. Here we consider the problem of deciding if there exists a binary level-1 phylogenetic network displaying a given set T of binary binets or trinets over a taxon set X, and constructing such a network whenever it exists. We show that this is NP-hard for trinets but polynomial-time solvable for binets. Moreover, we show that the problem is still polynomial-time solvable for inputs consisting of binets and trinets as long as the cycles in the trinets have size three. Finally, we present an O(3^{|X|} poly(|X|)) time algorithm for general sets of binets and trinets. The latter two algorithms generalise to instances containing level-1 networks with arbitrarily many leaves, and thus provide some of the first supernetwork algorithms for computing networks from a set of rooted 1 phylogenetic networks

Gene Order Phylogeny of the Genus Prochlorococcus

Using gene order as a phylogenetic character has the potential to resolve previously unresolved species relationships. This character was used to resolve the evolutionary history within the genus Prochlorococcus, a group of marine cyanobacteria.Orthologous gene sets and their genomic positions were identified from 12 species of Prochlorococcus and 1 outgroup species of Synechococcus. From this data, inversion and breakpoint distance-based phylogenetic trees were computed by GRAPPA and FastME. Statistical support of the resulting topology was obtained by application of a 50% jackknife resampling technique. The result was consistent and congruent with nucleotide sequence-based and gene-content based trees. Also, a previously unresolved clade was resolved, that of MIT9211 and SS120.This is the first study to use gene order data to resolve a bacterial phylogeny at the genus level. It suggests that the technique is useful in resolving the Tree of Life

Towards a Processual Microbial Ontology

types: ArticleStandard microbial evolutionary ontology is organized according to a nested hierarchy of entities at various levels of biological organization. It typically detects and defines these entities in relation to the most stable aspects of evolutionary processes, by identifying lineages evolving by a process of vertical inheritance from an ancestral entity. However, recent advances in microbiology indicate that such an ontology has important limitations. The various dynamics detected within microbiological systems reveal that a focus on the most stable entities (or features of entities) over time inevitably underestimates the extent and nature of microbial diversity. These dynamics are not the outcome of the process of vertical descent alone. Other processes, often involving causal interactions between entities from distinct levels of biological organisation, or operating at different time scales, are responsible not only for the destabilisation of pre-existing entities, but also for the emergence and stabilisation of novel entities in the microbial world. In this article we consider microbial entities as more or less stabilised functional wholes, and sketch a network-based ontology that can represent a diverse set of processes including, for example, as well as phylogenetic relations, interactions that stabilise or destabilise the interacting entities, spatial relations, ecological connections, and genetic exchanges. We use this pluralistic framework for evaluating (i) the existing ontological assumptions in evolution (e.g. whether currently recognized entities are adequate for understanding the causes of change and stabilisation in the microbial world), and (ii) for identifying hidden ontological kinds, essentially invisible from within a more limited perspective. We propose to recognize additional classes of entities that provide new insights into the structure of the microbial world, namely ‘‘processually equivalent’’ entities, ‘‘processually versatile’’ entities, and ‘‘stabilized’’ entities.Economic and Social Research Council, U

Binets: fundamental building blocks for phylogenetic networks

Phylogenetic networks are a generalization of evolutionary trees that are used by biologists to represent the evolution of organisms which have undergone reticulate evolution. Essentially, a phylogenetic network is a directed acyclic graph having a unique root in which the leaves are labelled by a given set of species. Recently, some approaches have been developed to construct phylogenetic networks from collections of networks on 2- and 3-leaved networks, which are known as binets and trinets, respectively. Here we study in more depth properties of collections of binets, one of the simplest possible types of networks into which a phylogenetic network can be decomposed. More speci_cally, we show that if a collection of level-1 binets is compatible with some binary network, then it is also compatible with a binary level-1 network. Our proofs are based on useful structural results concerning lowest stable ancestors in networks. In addition, we show that, although the binets do not determine the topology of the network, they do determine the number of reticulations in the network, which is one of its most important parameters. We also consider algorithmic questions concerning binets. We show that deciding whether an arbitrary set of binets is compatible with some network is at least as hard as the well-known Graph Isomorphism problem. However, if we restrict to level-1 binets, it is possible to decide in polynomial time whether there exists a binary network that displays all the binets. We also show that to _nd a network that displays a maximum number of the binets is NP-hard, but that there exists a simple polynomial-time 1/3-approximation algorithm for this problem. It is hoped that these results will eventually assist in the development of new methods for constructing phylogenetic networks from collections of smaller networks

GO4genome: A Prokaryotic Phylogeny Based on Genome Organization

Determining the phylogeny of closely related prokaryotes may fail in an analysis of rRNA or a small set of sequences. Whole-genome phylogeny utilizes the maximally available sample space. For a precise determination of genome similarity, two aspects have to be considered when developing an algorithm of whole-genome phylogeny: (1) gene order conservation is a more precise signal than gene content; and (2) when using sequence similarity, failures in identifying orthologues or the in situ replacement of genes via horizontal gene transfer may give misleading results. GO4genome is a new paradigm, which is based on a detailed analysis of gene function and the location of the respective genes. For characterization of genes, the algorithm uses gene ontology enabling a comparison of function independent of evolutionary relationship. After the identification of locally optimal series of gene functions, their length distribution is utilized to compute a phylogenetic distance. The outcome is a classification of genomes based on metabolic capabilities and their organization. Thus, the impact of effects on genome organization that are not covered by methods of molecular phylogeny can be studied. Genomes of strains belonging to Escherichia coli, Shigella, Streptococcus, Methanosarcina, and Yersinia were analyzed. Differences from the findings of classical methods are discussed

Nucleocytoplasmic transport: a thermodynamic mechanism

The nuclear pore supports molecular communication between cytoplasm and nucleus in eukaryotic cells. Selective transport of proteins is mediated by soluble receptors, whose regulation by the small GTPase Ran leads to cargo accumulation in, or depletion from the nucleus, i.e., nuclear import or nuclear export. We consider the operation of this transport system by a combined analytical and experimental approach. Provocative predictions of a simple model were tested using cell-free nuclei reconstituted in Xenopus egg extract, a system well suited to quantitative studies. We found that accumulation capacity is limited, so that introduction of one import cargo leads to egress of another. Clearly, the pore per se does not determine transport directionality. Moreover, different cargo reach a similar ratio of nuclear to cytoplasmic concentration in steady-state. The model shows that this ratio should in fact be independent of the receptor-cargo affinity, though kinetics may be strongly influenced. Numerical conservation of the system components highlights a conflict between the observations and the popular concept of transport cycles. We suggest that chemical partitioning provides a framework to understand the capacity to generate concentration gradients by equilibration of the receptor-cargo intermediary.Comment: in press at HFSP Journal, vol 3 16 text pages, 1 table, 4 figures, plus Supplementary Material include

A Strong Deletion Bias in Nonallelic Gene Conversion

Gene conversion is the unidirectional transfer of genetic information between orthologous (allelic) or paralogous (nonallelic) genomic segments. Though a number of studies have examined nucleotide replacements, little is known about length difference mutations produced by gene conversion. Here, we investigate insertions and deletions produced by nonallelic gene conversion in 338 Drosophila and 10,149 primate paralogs. Using a direct phylogenetic approach, we identify 179 insertions and 614 deletions in Drosophila paralogs, and 132 insertions and 455 deletions in primate paralogs. Thus, nonallelic gene conversion is strongly deletion-biased in both lineages, with almost 3.5 times as many conversion-induced deletions as insertions. In primates, the deletion bias is considerably stronger for long indels and, in both lineages, the per-site rate of gene conversion is orders of magnitudes higher than that of ordinary mutation. Due to this high rate, deletion-biased nonallelic gene conversion plays a key role in genome size evolution, leading to the cooperative shrinkage and eventual disappearance of selectively neutral paralogs