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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. 

Abstract The evolution of multicellularity represents a major transition in life’s history, enabling the rise of complex organisms. Multicellular groups can evolve through multiple developmental modes, but a common step is the formation of permanent cell–cell attachments after division. The characteristics of the multicellular morphology that emerges have profound consequences for the subsequent evolution of a nascent multicellular lineage, but little prior work has investigated these dynamics directly. Here, we examine a widespread yet understudied emergent multicellular morphology: cuboidal packing. Extinct and extant multicellular organisms across the tree of life have evolved to form groups in which spherical cells divide but remain attached, forming approximately cubic subunits. To experimentally investigate the evolution of cuboidal cell packing, we used settling selection to favor the evolution of simple multicellularity in unicellular, spherical Schizosaccharomyces pombe yeast. Multicellular clusters with cuboidal organization rapidly evolved, displacing the unicellular ancestor. These clusters displayed key hallmarks of an evolutionary transition in individuality: groups possess an emergent life cycle driven by physical fracture, group size is heritable, and they respond to group-level selection via multicellular adaptation. In 2 out of 5 lineages, group formation was driven by mutations in the ace2 gene, preventing daughter cell separation after division. Remarkably, ace2 mutations also underlie the transition to multicellularity in Saccharomyces cerevisiae and Candida glabrata, lineages that last shared a common ancestor >300 million years ago. Our results provide insight into the evolution of cuboidal cell packing, an understudied multicellular morphology, and highlight the deeply convergent potential for a transition to multicellular individuality within fungi. 

The evolution of multicellular life spurred evolutionary radiations, fundamentally changing many of Earth’s ecosystems. Yet little is known about how early steps in the evolution of multicellularity affect eco-evolutionary dynamics. Through long-term experimental evolution, we observed niche partitioning and the adaptive divergence of two specialized lineages from a single multicellular ancestor. Over 715 daily transfers, snowflake yeast were subjected to selection for rapid growth, followed by selection favouring larger group size. Small and large cluster-forming lineages evolved from a monomorphic ancestor, coexisting for over ~4,300 generations, specializing on divergent aspects of a trade-off between growth rate and survival. Through modelling and experimentation, we demonstrate that coexistence is maintained by a trade-off between organismal size and competitiveness for dissolved oxygen. Taken together, this work shows how the evolution of a new level of biological individuality can rapidly drive adaptive diversification and the expansion of a nascent multicellular niche, one of the most historically impactful emergent properties of this evolutionary transition. 

Abstract Resilient landscapes have helped maintain terrestrial biodiversity during periods of climatic and environmental change. Identifying the tempo and mode of landscape transitions and the drivers of landscape resilience is critical to maintaining natural systems and preserving biodiversity given today's rapid climate and land use changes. However, resilient landscapes are difficult to recognize on short time scales, as perturbations are challenging to quantify and ecosystem transitions are rare. Here we analyze two components of North American landscape resilience over 20,000 years: residence time and recovery time. To evaluate landscape dynamics, we use plant biomes, preserved in the fossil pollen record, to examine how long a biome type persists at a given site (residence time) and how long it takes for the biome at that site to reestablish following a transition (recovery time). Biomes have a median residence time of only 230–460 years. Only 64% of biomes recover their original biome type, but recovery time is 140–290 years. Temperatures changing faster than 0.5°C per 500 years result in much reduced residence times. Following a transition, biodiverse biomes reestablish more quickly. Landscape resilience varies through time. Notably, short residence times and long recovery times directly preceded the end‐Pleistocene megafauna extinction, resulting in regional destabilization, and combining with more proximal human impacts to deliver a one‐two punch to megafauna species. Our work indicates that landscapes today are once again exhibiting low resilience, foreboding potential extinctions to come. Conservation strategies focused on improving both landscape and ecosystem resilience by increasing local connectivity and targeting regions with high richness and diverse landforms can mitigate these extinction risks.