A fundamental problem in biology is the evolutionary transition from single cells to multicellular life forms. During this transition the unit of selection shifts from individual cells to groups of ...cooperating cells. Although there is much theory, there are few empirical studies. Here we describe an evolutionary transition that occurs in experimental populations of Pseudomonas fluorescens propagated in a spatially heterogeneous environment. Cooperating groups are formed by over-production of an adhesive polymer, which causes the interests of individuals to align with those of the group. The costs and benefits of cooperation, plus evolutionary susceptibility to defecting genotypes, were analysed to determine conformation to theory. Cooperation was costly to individuals, but beneficial to the group. Defecting genotypes evolved in populations founded by the cooperating type and were fitter in the presence of this type than in its absence. In the short term, defectors sabotaged the viability of the group; but these findings nevertheless show that transitions to higher orders of complexity are readily achievable, provide insights into the selective conditions, and facilitate experimental analysis of the evolution of individuality.
That humans might undergo future evolutionary transitions in individuality (ETIs) seems fanciful. However, drawing upon recent thinking concerning the origins of properties that underpin ETIs, I ...argue that certain ETIs are imminently realizable. Central to my argument is recognition that heritable variance in fitness at higher levels of organization can be externally imposed (scaffolded) by specific ecological structures and cultural practices. While ETIs to eusociality seem highly improbable, ETIs involving symbioses between humans and artificial intelligence (AI) can be readily envisaged. A necessary requirement is that fitness-affecting interactions between humans and AI devices are inherited by offspring. The Mendelian nature of human reproduction ensures that offspring resemble parents. Reproduction of AI devices requires nothing more than transference of algorithms from parental AI devices to devices that are assigned to offspring. This simple copying, combined with societal structures that require humans to carry AI devices, ensures heritable variance in fitness at the level of both interacting partners. Selection at the collective level will drive alignment of replicative fates and increase co-dependency, thus alleviating need for continual imposition of externally imposed scaffolds. I conclude by drawing attention to the immediacy of such transitions and express concern over possibilities for malevolent manipulation. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.
Studies of microbial evolutionary dynamics are being transformed by the availability of affordable high-throughput sequencing technologies, which allow whole-genome sequencing of hundreds of related ...taxa in a single study. Reconstructing a phylogenetic tree of these taxa is generally a crucial step in any evolutionary analysis. Instead of constructing genome assemblies for all taxa, annotating these assemblies, and aligning orthologous genes, many recent studies 1) directly map raw sequencing reads to a single reference sequence, 2) extract single nucleotide polymorphisms (SNPs), and 3) infer the phylogenetic tree using maximum likelihood methods from the aligned SNP positions. However, here we show that, when using such methods to reconstruct phylogenies from sets of simulated sequences, both the exclusion of nonpolymorphic positions and the alignment to a single reference genome, introduce systematic biases and errors in phylogeny reconstruction. To address these problems, we developed a new method that combines alignments from mappings to multiple reference sequences and show that this successfully removes biases from the reconstructed phylogenies. We implemented this method as a web server named REALPHY (Reference sequence Alignment-based Phylogeny builder), which fully automates phylogenetic reconstruction from raw sequencing reads.
Oxidative stress is a major cause of mutation but little is known about how growth in the absence of oxygen impacts the rate and spectrum of mutations. We employed long-term mutation accumulation ...experiments to directly measure the rates and spectra of spontaneous mutation events in Escherichia coli populations propagated under aerobic and anaerobic conditions. To detect mutations, whole genome sequencing was coupled with methods of analysis sufficient to identify a broad range of mutational classes, including structural variants (SVs) generated by movement of repetitive elements. The anaerobically grown populations displayed a mutation rate nearly twice that of the aerobic populations, showed distinct asymmetric mutational strand biases, and greater insertion element activity. Consistent with mutation rate and spectra observations, genes for transposition and recombination repair associated with SVs were up-regulated during anaerobic growth. Together, these results define differences in mutational spectra affecting the evolution of facultative anaerobes.
Cooperation is central to the emergence of multicellular life; however, the means by which the earliest collectives (groups of cells) maintained integrity in the face of destructive cheating types is ...unclear. One idea posits cheats as a primitive germ line in a life cycle that facilitates collective reproduction. Here we describe an experiment in which simple cooperating lineages of bacteria were propagated under a selective regime that rewarded collective-level persistence. Collectives reproduced via life cycles that either embraced, or purged, cheating types. When embraced, the life cycle alternated between phenotypic states. Selection fostered inception of a developmental switch that underpinned the emergence of collectives whose fitness, during the course of evolution, became decoupled from the fitness of constituent cells. Such development and decoupling did not occur when groups reproduced via a cheat-purging regime. Our findings capture key events in the evolution of Darwinian individuality during the transition from single cells to multicellularity.
Integrative mobile genetic elements (MGEs), such as transposons and insertion sequences, propagate within bacterial genomes, but persistence times in individual lineages are short. For long‐term ...survival, MGEs must continuously invade new hosts by horizontal transfer. Theoretically, MGEs that persist for millions of years in single lineages, and are thus subject to vertical inheritance, should not exist. Here we draw attention to an exception – a class of MGE termed REPIN. REPINs are non‐autonomous MGEs whose duplication depends on non‐jumping RAYT transposases. Comparisons of REPINs and typical MGEs show that replication rates of REPINs are orders of magnitude lower, REPIN population size fluctuations correlate with changes in available genome space, REPIN conservation depends on RAYT function, and REPIN diversity accumulates within host lineages. These data lead to the hypothesis that REPINs form enduring, beneficial associations with eubacterial chromosomes. Given replicative nesting, our hypothesis predicts conflicts arising from the diverging effects of selection acting simultaneously on REPINs and host genomes. Evidence in support comes from patterns of REPIN abundance and diversity in two distantly related bacterial species. Together this bolsters the conclusion that REPINs are the genetic counterpart of mutualistic endosymbiotic bacteria.
REPINs are mobile genetic elements that have evolved from the terminal repeats of a parasitic transposon and replicate by virtue of interaction with RAYTs. Uniquely, the REPIN‐RAYT system is widespread among eubacteria, has persisted for millions of years, is vertically transmitted – therefore beneficial to hosts – and reminiscent of mutualistic endosymbionts.
Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using ...mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (
) that arises from density-dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.
The effect of population structure on the rate of evolution Frean, Marcus; Rainey, Paul B.; Traulsen, Arne
Proceedings - Royal Society. Biological sciences/Proceedings - Royal Society. Biological Sciences,
07/2013, Volume:
280, Issue:
1762
Journal Article
Peer reviewed
Open access
Ecological factors exert a range of effects on the dynamics of the evolutionary process. A particularly marked effect comes from population structure, which can affect the probability that new ...mutations reach fixation. Our interest is in population structures, such as those depicted by ‘star graphs’, that amplify the effects of selection by further increasing the fixation probability of advantageous mutants and decreasing the fixation probability of disadvantageous mutants. The fact that star graphs increase the fixation probability of beneficial mutations has lead to the conclusion that evolution proceeds more rapidly in star-structured populations, compared with mixed (unstructured) populations. Here, we show that the effects of population structure on the rate of evolution are more complex and subtle than previously recognized and draw attention to the importance of fixation time. By comparing population structures that amplify selection with other population structures, both analytically and numerically, we show that evolution can slow down substantially even in populations where selection is amplified.
Reproduction is a defining feature of living systems. To reproduce, aggregates of biological units (e.g., multicellular organisms or colonial bacteria) must fragment into smaller parts. Fragmentation ...modes in nature range from binary fission in bacteria to collective-level fragmentation and the production of unicellular propagules in multicellular organisms. Despite this apparent ubiquity, the adaptive significance of fragmentation modes has received little attention. Here, we develop a model in which groups arise from the division of single cells that do not separate but stay together until the moment of group fragmentation. We allow for all possible fragmentation patterns and calculate the population growth rate of each associated life cycle. Fragmentation modes that maximise growth rate comprise a restrictive set of patterns that include production of unicellular propagules and division into two similar size groups. Life cycles marked by single-cell bottlenecks maximise population growth rate under a wide range of conditions. This surprising result offers a new evolutionary explanation for the widespread occurrence of this mode of reproduction. All in all, our model provides a framework for exploring the adaptive significance of fragmentation modes and their associated life cycles.
Eukaryotes and prokaryotes have distinct genome architectures, with marked differences in genome size, the ratio of coding/non-coding DNA, and the abundance of transposable elements (TEs). As TEs ...replicate independently of their hosts, the proliferation of TEs is thought to have driven genome expansion in eukaryotes. However, prokaryotes also have TEs in intergenic spaces, so why do prokaryotes have small, streamlined genomes? Using an
model describing the genomes of single-celled asexual organisms that coevolve with TEs, we show that TEs acquired from the environment by horizontal gene transfer can promote the evolution of genome streamlining. The process depends on local interactions and is underpinned by rock-paper-scissors dynamics in which populations of cells with streamlined genomes beat TEs, which beat non-streamlined genomes, which beat streamlined genomes, in continuous and repeating cycles. Streamlining is maladaptive to individual cells, but improves lineage viability by hindering the proliferation of TEs. Streamlining does not evolve in sexually reproducing populations because recombination partially frees TEs from the deleterious effects they cause. This article is part of the theme issue 'The secret lives of microbial mobile genetic elements'.
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