Biology subjects

Pichugin, Y.

Publications and source records attributed to Pichugin, Y..

13 recordsLinked to original sources

bioRxiv2026

Evolution of informed dispersal strategies in trophic meta-communities

Living organisms move and their movement is both a response to local conditions and, often, the cause of change in those conditions. This feedback loop is often overlooked in theoretical studies on the evolution of dispersal, which assume that either the decision to leave is uninformed or that the local conditions are exogenously driven. Here, we embrace the feedback loop and study what dispersal strategies evolve in a trophic meta-population where the dynamics are entirely endogenous. We show that there are five possible classes of strategies that can evolve depending on the ecological conditions: leaving once local conditions fall low enough (Unsaturated), having an extended stay even under adverse conditions (Saturated), leaving from a high quality location (Anxious), leaving independently of the location state (Ignorant), and completely abstaining from dispersal (No-dispersal). The Unsaturated class captures the classical prediction of the marginal value theorem, while the other four extend the range of possible evolutionarily optimal strategies. Which class of strategies evolves depends on the kind of information being sensed (resource availability versus conspecifics density), the size of the local consumer population at equilibrium, and the stability of this equilibrium. Our results provide a theoretical underpinning for the diversity of movement strategies observed in nature that deviate from classic predictions and suggest a comparative framework that can inform experimental design.

evolutionary biology↗

bioRxiv2022

Eco-evolutionary dynamics of clonal multicellular life cycles

The evolution of multicellular life cycles is a central process in the course of the emergence of multicellularity. The simplest multicellular life cycle is comprised from the growth of the propagule into a colony and its fragmentation to give rise to new propagules. The majority of theoretical models assume selection among life cycles to be driven by internal properties of multicellular groups resulting in growth competition. At the same time, the influence of interactions between groups on the evolution of life cycles is rarely even considered. Here, we present a model of colonial life cycles evolution taking into account group interactions. Our work shows that the outcome of evolution could be coexistence between multiple life cycles or that the outcome may depend on the initial state of the population - scenarios impossible without group interactions. At the same time, we found that some results of these simpler models remain relevant: Evolutionary stable strategies in our model are restricted to binary fragmentation - the same class of life cycles which contains all evolutionarily optimal life cycles in the model without interactions. Our results demonstrate that while models neglecting interactions can capture short-term dynamics, they fall short in predicting the population-scale picture of the evolution.

evolutionary biology↗

bioRxiv2021

Phenotypic plasticity, life cycles and the evolutionary transition to multicellularity

SUMMARYUnderstanding the evolutionary transition to multicellularity is a key problem in evolutionary biology (1-4). While around 25 independent instances of the evolution of multicellular existence are known across the tree of life (5), the ecological conditions that drive such transformations are not well understood. The first known transition to multicellularity occurred approximately 2.5 billion years ago in cyanobacteria (5-7), and todays cyanobacteria are characterized by an enormous morphological diversity, based upon which they have been classified into five sections. They range from single-celled species (section I), unicellular cyanobacteria with packet-like phenotypes, e.g., tetrads (section II) and simple filamentous species (section III) to highly differentiated filamentous ones (sections IV and V) (8-10). The unicellular cyanobacterium Cyanothece sp. ATCC 51142, an isolate from the intertidal zone of the U.S. Gulf Coast (11), has been classified as a section I species, and it phylogenetically clusters with the other N2-fixing unicellular cyanobacteria (12). Here we report a facultative multicellular life cycle for a unicellular cyanobacterium, where multicellular filaments and unicellular stages alternate. In a series of experiments we identify the environmental factors underlying the phenotypic switch between the two morphologies. Then we experimentally confirm that the dissolution of filaments into solitary cells is triggered by changes in the external environment, which in turn is modified by the Cyanothece cells. Finally, using numerical models, we test a number of hypotheses regarding the nature of the environmental cues and the physical mechanisms underlying filament dissolution. While results predict that the observed response can be caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in (13,14)). The best-fit modeling results demonstrate a nonlinear effect of the compound, which is characteristic for density-dependent sensing systems (15,16). Further, filament fragmentation is predicted to occur by means of connection cleavage rather than by cell death of every alternate cell, which is corroborated by results from fluorescent and scanning electron microscopy. The phenotypic switch between the single-celled and multicellular morphology constitutes an environmentally dependent life cycle, which likely represents an important step en route to permanent multicellularity.

evolutionary biology↗

bioRxiv2021

Evolution of reproductive strategies in incipient multicellularity

Multicellular organisms can potentially show a large degree of diversity in reproductive strategies, as they could reproduce offspring with varying sizes and compositions compared to their unicellular ancestors. In reality, only a few of these reproductive strategies are prevalent. To understand why this could be the case, we develop a stage-structured population model to probe the evolutionary growth advantages of reproductive strategies in incipient multicellular organisms. The performance of reproductive strategies is evaluated by the growth rates of corresponding populations. We identify the optimal reproductive strategy, which leads to the largest growth rate for a population. Considering the effects of organism size and cellular interaction, we found that distinct reproductive strategies could perform uniquely or equally well under different conditions. Only binary-splitting reproductive strategies can be uniquely optimal. Our results show that organism size and cellular interaction can play crucial roles in shaping reproductive strategies in nascent multicellularity. Our model sheds light on understanding the mechanism driving the evolution of reproductive strategies in incipient multicellularity. Meanwhile, beyond multicellularity, our results imply a crucial factor in the evolution of reproductive strategies of unicellular species - organism size.

evolutionary biology↗

bioRxiv2021

Principles of ecDNA random inheritance drive rapid genome change and therapy resistance in human cancers

The foundational principles of Darwinian evolution are variation, selection, and identity by descent. Oncogene amplification on extrachromosomal DNA (ecDNA) is a common event, driving aggressive tumour growth, drug resistance, and shorter survival in patients1-4. Currently, the impact of non-chromosomal oncogene inheritance--random identity by descent--is not well understood. Neither is the impact of ecDNA on variation and selection. Here, integrating mathematical modeling, unbiased image analysis, CRISPR-based ecDNA tagging, and live-cell imaging, we identify a set of basic "rules" for how random ecDNA inheritance drives oncogene copy number and distribution, resulting in extensive intratumoural ecDNA copy number heterogeneity and rapid adaptation to metabolic stress and targeted cancer treatment. Observed ecDNAs obligatorily benefit host cell survival or growth and can change within a single cell cycle. In studies ranging from well-curated, patient-derived cancer cell cultures to clinical tumour samples from patients with glioblastoma and neuroblastoma treated with oncogene-targeted drugs, we show how these ecDNA inheritance "rules" can predict, a priori, some of the aggressive features of ecDNA-containing cancers. These properties are entailed by their ability to rapidly change their genomes in a way that is not possible for cancers driven by chromosomal oncogene amplification. These results shed new light on how the non-chromosomal random inheritance pattern of ecDNA underlies poor outcomes for cancer patients.

cancer biology↗

bioRxiv2021

Evolution of irreversible somatic differentiation

A key innovation emerging in complex animals is irreversible somatic differentiation: daughters of a vegetative cell perform a vegetative function as well, thus, forming a somatic lineage that can no longer be directly involved in reproduction. Primitive species use a different strategy: vegetative and reproductive tasks are separated in time rather than in space. Starting from such a strategy, how is it possible to evolve life forms which use some of their cells exclusively for vegetative functions? Here, we developed an evolutionary model of development of a simple multicellular organism and found that three components are necessary for the evolution of irreversible somatic differentiation: (i) costly cell differentiation, (ii) vegetative cells that significantly improve the organisms performance even if present in small numbers, and (iii) large enough organism size. Our findings demonstrate how an egalitarian development typical for loose cell colonies can evolve into germ-soma differentiation dominating metazoans.

evolutionary biology↗

bioRxiv2020

Why is cyclic dominance so rare?

Natural populations can contain multiple types of coexisting individuals. How does natural selection maintain such diversity within and across populations? A popular theoretical basis for the maintenance of diversity is cyclic dominance, illustrated by the rock-paper-scissor game. However, it appears difficult to find cyclic dominance in nature. Why is this case? Focusing on continuously produced novel mutations, we theoretically addressed the rareness of cyclic dominance. We developed a model of an evolving population and studied the formation of cyclic dominance. Our results showed that the chance for cyclic dominance to emerge is lower when the newly introduced type is similar to existing types, whereas the introduction of an unrelated type improves these chances. This suggests that cyclic dominance is more likely to evolve through the assembly of unrelated types whereas it rarely evolves within a community of similar types.

evolutionary biology↗

bioRxiv2019

Stochastic dynamics of extra-chromosomal DNA

Nuclear extra-chromosomal DNA (ecDNA) is highly prevalent in human tumours. ecDNA amplifications can promote accessible chromatin, oncogen over-expression and imply a worse clinical prognosis. Yet, little is known about the evolutionary process of ecDNA in human cancers. Here, we develop the theoretical foundation of the ecDNA somatic evolutionary process combining mathematical, computational and experimental approaches. We show that random ecDNA segregation leads to unintuitive dynamics even if ecDNA is under very strong positive selection. Patterns of inter- and intra-tumour ecDNA and chromosomal heterogeneity differ markedly and standard approaches are not directly applicable to quantify ecDNA evolution. We show that evolutionary informed modelling leads to testable predictions on how to distinguish positively selected from neutral ecDNA dynamics. Our predictions describe the dynamics of circular amplicons in GBM39 cell line experiments, suggesting a 300% fitness increase due to circular extra-chromosomal EGFRvIII amplifications. Our work lies the basis for further studies to quantitate ecDNA somatic evolutionary processes.

cancer biology↗

bioRxiv2019

Evolution of simple multicellular life cycles in dynamic environments

The mode of reproduction is a critical characteristic of any species, as it has a strong effect on its evolution. As any other trait, the reproduction mode is subject to natural selection and may adapt to the environment. When the environment varies over time, different reproduction modes could be optimal at different times. The natural response to a dynamic environment seems to be bet hedging, where multiple reproductive strategies are stochastically executed. Here, we develop a framework for the evolution of simple multicellular life cycles in a dynamic environment. We use a matrix population model of undifferentiated multicellular groups undergoing fragmentation and ask which mode maximizes the population growth rate. Counterintuitively, we find that natural selection in dynamic environments generally tends to promote deterministic, not stochastic, reproduction modes.

evolutionary biology↗

bioRxiv2019

Interacting cells driving the evolution of multicellular life cycles

Evolution of complex multicellular life begun from the emergence of life cycle involving formation of cell clusters. Opportunity for cells to interact within clusters provided them an advantage over unicellular life forms. However, what kind of interactions may lead to the evolution of multicellular life cycles? Here, we combine evolutionary game theory with a model for the emergence of multicellular groups to investigate how cell interactions can influence reproduction modes during the early stages of the evolution of multicellularity. We identify evolutionary optimal life cycles as those which maximize the population growth rate. Among all interactions captured by two-player games, only eight life cycles were found to be evolutionarily optimal. Moreover, the vast majority of games promotes either of two classes of life cycles: (i) splitting into unicellular propagules or (ii) fragmentation into two offspring clusters of equal (or almost equal) size. Our findings indicate that the three most important characteristics, determining whether multicellular life cycles will evolve, are average performance of homogeneous groups, heterogeneous groups, and solitary cells.

evolutionary biology↗

bioRxiv2018

Stochastic population dynamics driven by mutant interactors

Spontaneous random mutations are an important source of variation in populations. Many evolutionary models consider mutants with a fixed fitness chosen from a certain fitness distribution without considering any interactions among the residents and mutants. Here, we go beyond this and consider \"mutant interactors\", which lead to new interactions between the residents and invading mutants that can affect the carrying capacity and the extinction risk of populations. We model microscopic interactions between individuals by using a dynamical payoff matrix and analyze the stochastic dynamics of such populations. New interactions drawn from invading mutants can drive the population away from the previous equilibrium, and lead to changes in the population size -- the population size is an evolving property rather than a fixed number or externally controlled variable. We present analytical results for the average population size over time and quantify the extinction risk of the population by the mean time to extinction.

evolutionary biology↗

bioRxiv2018

Reproduction costs can drive the evolution of groups

A fascinating wealth of life cycles is observed in biology, from unicellularity to the concerted fragmentation of multi-cellular units. However, the understanding of factors driving the evolution of life cycles is still limited. We investigate how reproduction costs influence this process. We consider a basic model of a group structured population of undifferentiated cells, where groups reproduce by fragmentation. Fragmentation events are associated with a cost expressed by either a fragmentation delay, a fragmentation risk, or a fragmentation loss. The introduction of such fragmentation costs vastly increases the set of potentially optimal life cycles. Based on these findings, we suggest that the evolution of life cycles and the splitting into multiple offspring can be directly associated with the fragmentation cost. Moreover, the impact of this cost alone is strong enough to drive the emergence of multicellular groups, even under scenarios that strongly disfavour groups compared to solitary individuals.

evolutionary biology↗

bioRxiv2017

Fragmentation Modes And The Evolution Of Life Cycles

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.\n\nAuthor SummaryMode of reproduction is a defining trait of all organisms, including colonial bacteria and multicellular organisms. To produce offspring, aggregates must fragment by splitting into two or more groups. The particular way that a given group fragments defines the life cycle of the organism. For instance, insect colonies can reproduce by splitting or by producing individuals that found new colonies. Similarly, some colonial bacteria propagate by fission or by releasing single cells, while others split in highly sophisticated ways; in multicellular organisms reproduction typically proceeds via a single cell bottleneck phase. The space of possibilities for fragmentation is so vast that an exhaustive analysis seems daunting. Focusing on fragmentation modes of a simple kind we parametrise all possible modes of group fragmentation and identify those modes leading to the fastest population growth rate. Two kinds of life cycle dominate: one involving division into two equal size groups, and the other involving production of a unicellular propagule. The prevalence of these life cycles in nature is consistent with our null model and suggests that benefits accruing from population growth rate alone may have shaped the evolution of fragmentation mode.

evolutionary biology↗