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1. Topological constraints in early multicellularity favor reproductive division of labor

   https://doi.org/10.7554/eLife.54348  

   Yanni, David; Jacobeen, Shane; Márquez-Zacarías, Pedro; Weitz, Joshua S; Ratcliff, William C; Yunker, Peter J (September 2020, eLife)

   null (Ed.)

   Reproductive division of labor (e.g. germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e. productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e. productivity is a concave function of specialization). Through analytical theory and evolutionary individual-based simulations, we demonstrate that reproductive specialization is strongly favored in sparse networks of cellular interactions that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization. 

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2. Mosaic of Somatic Mutations in Earth’s Oldest Living Organism, Pando

   https://doi.org/10.1101/2024.10.19.619233  

   Pineau, Rozenn M; Mock, Karen E; Morris, Jesse; Kraklow, Vachel; Brunelle, Andrea; Pageot, Aurore; Ratcliff, William C; Gompert, Zachariah (October 2024, bioRxiv)

   Understanding how mutations arise and spread through individuals and populations is fundamental to evolutionary biology. Most organisms have a life cycle with unicellular bottlenecks during reproduction. However, some organisms like plants, fungi, or colonial animals can grow indefinitely, changing the manner in which mutations spread throughout both the individual and the population. Furthermore, clonally reproducing organisms may also achieve exceedingly long lifespans, making somatic mutation an important mechanism of creating heritable variation for Darwinian evolution by natural selection. Yet, little is known about intra-organism mutation rates and evolutionary trajectories in long-lived species. Here, we study the Pando aspen clone, the largest known quaking aspen (Populus tremuloides) clone founded by a single seedling and thought to be one of the oldest studied organisms. Aspen reproduce vegetatively via new root-borne stems forming clonal patches, sometimes spanning several hectares. To study the evolutionary history of the Pando clone, we collected and sequenced over 500 samples from Pando and neighboring clones, as well as from various tissue types within Pando, including leaves, roots, and bark. We applied a series of filters to distinguish somatic mutations from the pool of both somatic and germline mutations, incorporating a technical replicate sequencing approach to account for uncertainty in somatic mutation detection. Despite root spreading being spatially constrained, we observed only a modest positive correlation between genetic and spatial distance, suggesting the presence of a mechanism preventing the accumulation and spread of mutations across units. Phylogenetic models estimate the age of the clone to between ~16,000-80,000 years. This age is generally corroborated by the near-continuous presence of aspen pollen in a lake sediment record collected from Fish Lake near Pando. Overall, this work enhances understanding of mutation accumulation and dispersal within and between ramets of long-lived, clonally-reproducing organisms. Significance StatementThis study enhances our understanding of evolutionary processes in long-lived clonal organisms by investigating somatic mutation accumulation and dispersal patterns within the iconic Pando aspen clone. The authors estimated the clone to be between 10,000 and 80,000 years old and uncovered a modest spatial genetic structure in the 42.6-hectare clone, suggesting localized mutation build-up rather than dispersal along tissue lineages. This work sheds light on an ancient organism and how plants may evolve to preserve genetic integrity in meristems fueling indefinite growth, with implications for our comprehension of adaptive strategies in long-lived perennials. 

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3. Phenotype Design Space Provides a Mechanistic Framework Relating Molecular Parameters to Phenotype Diversity Available for Selection

   https://doi.org/10.1007/s00239-023-10127-y  

   Savageau, Michael A. (August 2023, Journal of Molecular Evolution)

   Abstract Two long-standing challenges in theoretical population genetics and evolution are predicting the distribution of phenotype diversity generated by mutation and available for selection, and determining the interaction of mutation, selection and drift to characterize evolutionary equilibria and dynamics. More fundamental for enabling such predictions is the current inability to causally link genotype to phenotype. There are three major mechanistic mappings required for such a linking – genetic sequence to kinetic parameters of the molecular processes, kinetic parameters to biochemical system phenotypes, and biochemical phenotypes to organismal phenotypes. This article introduces a theoretical framework, the Phenotype Design Space (PDS) framework, for addressing these challenges by focusing on the mapping of kinetic parameters to biochemical system phenotypes. It provides a quantitative theory whose key features include (1) a mathematically rigorous definition of phenotype based on biochemical kinetics, (2) enumeration of the full phenotypic repertoire, and (3) functional characterization of each phenotype independent of its context-dependent selection or fitness contributions. This framework is built on Design Space methods that relate system phenotypes to genetically determined parameters and environmentally determined variables. It also has the potential to automate prediction of phenotype-specific mutation rate constants and equilibrium distributions of phenotype diversity in microbial populations undergoing steady-state exponential growth, which provides an ideal reference to which more realistic cases can be compared. Although the framework is quite general and flexible, the details will undoubtedly differ for different functions, organisms and contexts. Here a hypothetical case study involving a small molecular system, a primordial circadian clock, is used to introduce this framework and to illustrate its use in a particular case. The framework is built on fundamental biochemical kinetics. Thus, the foundation is based on linear algebra and reasonable physical assumptions, which provide numerous opportunities for experimental testing and further elaboration to deal with complex multicellular organisms that are currently beyond its scope. The discussion provides a comparison of results from the PDS framework with those from other approaches in theoretical population genetics. 

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4. The divergence of mutation rates and spectra across the Tree of Life

   https://doi.org/10.15252/embr.202357561  

   Lynch, Michael; Ali, Farhan; Lin, Tongtong; Wang, Yaohai; Ni, Jiahao; Long, Hongan (August 2023, EMBO reports)

   Abstract Owing to advances in genome sequencing, genome stability has become one of the most scrutinized cellular traits across the Tree of Life. Despite its centrality to all things biological, the mutation rate (per nucleotide site per generation) ranges over three orders of magnitude among species and several‐fold within individual phylogenetic lineages. Within all major organismal groups, mutation rates scale negatively with the effective population size of a species and with the amount of functional DNA in the genome. This relationship is most parsimoniously explained by the drift‐barrier hypothesis, which postulates that natural selection typically operates to reduce mutation rates until further improvement is thwarted by the power of random genetic drift. Despite this constraint, the molecular mechanisms underlying DNA replication fidelity and repair are free to wander, provided the performance of the entire system is maintained at the prevailing level. The evolutionary flexibility of the mutation rate bears on the resolution of several prior conundrums in phylogenetic and population‐genetic analysis and raises challenges for future applications in these areas. 

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5. Physiological mechanisms of stress-induced evolution

   https://doi.org/10.1242/jeb.243264  

   Mojica, Elizabeth A.; Kültz, Dietmar (March 2022, Journal of Experimental Biology)

   ABSTRACT Organisms mount the cellular stress response whenever environmental parameters exceed the range that is conducive to maintaining homeostasis. This response is critical for survival in emergency situations because it protects macromolecular integrity and, therefore, cell/organismal function. From an evolutionary perspective, the cellular stress response counteracts severe stress by accelerating adaptation via a process called stress-induced evolution. In this Review, we summarize five key physiological mechanisms of stress-induced evolution. Namely, these are stress-induced changes in: (1) mutation rates, (2) histone post-translational modifications, (3) DNA methylation, (4) chromoanagenesis and (5) transposable element activity. Through each of these mechanisms, organisms rapidly generate heritable phenotypes that may be adaptive, maladaptive or neutral in specific contexts. Regardless of their consequences to individual fitness, these mechanisms produce phenotypic variation at the population level. Because variation fuels natural selection, the physiological mechanisms of stress-induced evolution increase the likelihood that populations can avoid extirpation and instead adapt under the stress of new environmental conditions. 

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