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Publications (10 of 18) Show all publications
Pineau, R. M., Libby, E., Demory, D., Lac, D. T., Day, T. C., Bravo, P., . . . Ratcliff, W. C. (2024). Emergence and maintenance of stable coexistence during a long-term multicellular evolution experiment. Nature Ecology & Evolution
Open this publication in new window or tab >>Emergence and maintenance of stable coexistence during a long-term multicellular evolution experiment
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2024 (English)In: Nature Ecology & Evolution, E-ISSN 2397-334XArticle in journal (Refereed) Epub ahead of print
Abstract [en]

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.

Place, publisher, year, edition, pages
Nature Publishing Group, 2024
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-222583 (URN)10.1038/s41559-024-02367-y (DOI)001185269300002 ()38486107 (PubMedID)2-s2.0-85187680819 (Scopus ID)
Funder
NIH (National Institutes of Health), 5R35GM138030NIH (National Institutes of Health), 1R35GM138354-01
Available from: 2024-04-08 Created: 2024-04-08 Last updated: 2024-04-08
Souza, L. S., Solowiej-Wedderburn, J., Bonforti, A. & Libby, E. (2024). Modeling endosymbioses: insights and hypotheses from theoretical approaches. PLoS biology, 22(4), Article ID e3002583.
Open this publication in new window or tab >>Modeling endosymbioses: insights and hypotheses from theoretical approaches
2024 (English)In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 22, no 4, article id e3002583Article in journal (Refereed) Published
Abstract [en]

Endosymbiotic relationships are pervasive across diverse taxa of life, offering key avenues for eco-evolutionary dynamics. Although a variety of experimental and empirical frameworks have shed light on critical aspects of endosymbiosis, theoretical frameworks (mathematical models) are especially well-suited for certain tasks. Mathematical models can integrate multiple factors to determine the net outcome of endosymbiotic relationships, identify broad patterns that connect endosymbioses with other systems, simplify biological complexity, generate hypotheses for underlying mechanisms, evaluate different hypotheses, identify constraints that limit certain biological interactions, and open new lines of inquiry. This Essay highlights the utility of mathematical models in endosymbiosis research, particularly in generating relevant hypotheses. Despite their limitations, mathematical models can be used to address known unknowns and discover unknown unknowns.

Place, publisher, year, edition, pages
Public Library of Science (PLoS), 2024
National Category
Evolutionary Biology Mathematics
Identifiers
urn:nbn:se:umu:diva-223651 (URN)10.1371/journal.pbio.3002583 (DOI)001202784300001 ()38598454 (PubMedID)2-s2.0-85190351519 (Scopus ID)
Funder
Swedish Research Council, 2018-03630The Kempe Foundations, SMK21-0004The Kempe Foundations, JCK22-0026.1The Kempe Foundations, JCK-2129.2
Available from: 2024-04-23 Created: 2024-04-23 Last updated: 2024-04-23Bibliographically approved
Pentz, J. T., MacGillivray, K., DuBose, J. G., Conlin, P. L., Reinhardt, E., Libby, E. & Ratcliff, W. C. (2023). Evolutionary consequences of nascent multicellular life cycles. eLIFE, 12, Article ID e84336.
Open this publication in new window or tab >>Evolutionary consequences of nascent multicellular life cycles
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2023 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 12, article id e84336Article in journal (Refereed) Published
Abstract [en]

A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing 'snowflake' yeast (Δace2/∆ace2) and aggregative 'floc' yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift-a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.

Place, publisher, year, edition, pages
eLife Sciences Publications Ltd, 2023
Keywords
adaptation, biological individuality, evolutionary biology, experimental evolution, life cycles, major transitions in evolution, multicellularity, S. cerevisiae
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-216180 (URN)10.7554/eLife.84336 (DOI)37889142 (PubMedID)2-s2.0-85175272892 (Scopus ID)
Funder
NIH (National Institutes of Health), T32GM142616Swedish Research Council
Available from: 2023-11-10 Created: 2023-11-10 Last updated: 2023-11-10Bibliographically approved
Libby, E., Kempes, C. P. & Okie, J. G. (2023). Metabolic compatibility and the rarity of prokaryote endosymbioses. Proceedings of the National Academy of Sciences of the United States of America, 120(17), Article ID e2206527120.
Open this publication in new window or tab >>Metabolic compatibility and the rarity of prokaryote endosymbioses
2023 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 120, no 17, article id e2206527120Article in journal (Refereed) Published
Abstract [en]

The evolution of the mitochondria was a significant event that gave rise to the eukaryotic lineage and most large complex life. Central to the origins of the mitochondria was an endosymbiosis between prokaryotes. Yet, despite the potential benefits that can stem from a prokaryotic endosymbiosis, their modern occurrence is exceptionally rare. While many factors may contribute to their rarity, we lack methods for estimating the extent to which they constrain the appearance of a prokaryotic endosymbiosis. Here, we address this knowledge gap by examining the role of metabolic compatibility between a prokaryotic host and endosymbiont. We use genome-scale metabolic flux models from three different collections (AGORA, KBase, and CarveMe) to assess the viability, fitness, and evolvability of potential prokaryotic endosymbioses. We find that while more than half of host-endosymbiont pairings are metabolically viable, the resulting endosymbioses have reduced growth rates compared to their ancestral metabolisms and are unlikely to gain mutations to overcome these fitness differences. In spite of these challenges, we do find that they may be more robust in the face of environmental perturbations at least in comparison with the ancestral host metabolism lineages. Our results provide a critical set of null models and expectations for understanding the forces that shape the structure of prokaryotic life.

Place, publisher, year, edition, pages
Proceedings of the National Academy of Sciences (PNAS), 2023
Keywords
endosymbiosis, eukaryogenesis, evolution, metabolic model, prokaryote
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-207699 (URN)10.1073/pnas.2206527120 (DOI)37071674 (PubMedID)2-s2.0-85152971782 (Scopus ID)
Funder
Swedish Research Council
Available from: 2023-04-28 Created: 2023-04-28 Last updated: 2023-04-28Bibliographically approved
Isaksson, H., Brännström, Å. & Libby, E. (2023). Minor variations in multicellular life cycles have major effects on adaptation. PloS Computational Biology, 19(4), Article ID e1010698.
Open this publication in new window or tab >>Minor variations in multicellular life cycles have major effects on adaptation
2023 (English)In: PloS Computational Biology, ISSN 1553-734X, E-ISSN 1553-7358, Vol. 19, no 4, article id e1010698Article in journal (Refereed) Published
Abstract [en]

Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence multicellular adaptation. Yet, there is an underlying assumption that at some scale or categorization multicellular life cycles are similar in terms of their adaptive potential. Here, we consider this possibility by exploring adaptation in a class of simple multicellular life cycles of filamentous organisms that only differ in one respect, how many daughter filaments are produced. We use mathematical models and evolutionary simulations to show that despite the similarities, qualitatively different mutations fix. In particular, we find that mutations with a tradeoff between cell growth and group survival, i.e. "selfish" or "altruistic" traits, spread differently. Specifically, altruistic mutations more readily spread in life cycles that produce few daughters while in life cycles producing many daughters either type of mutation can spread depending on the environment. Our results show that subtle changes in multicellular life cycles can fundamentally alter adaptation.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-209284 (URN)10.1371/journal.pcbi.1010698 (DOI)000974421200004 ()37083675 (PubMedID)2-s2.0-85159546634 (Scopus ID)
Funder
Swedish Research Council, 2018-0363
Available from: 2023-06-08 Created: 2023-06-08 Last updated: 2024-05-20Bibliographically approved
Andersson, R., Isaksson, H. & Libby, E. (2022). Multi-species multicellular life cycles. In: The evolution of multicellularity: (pp. 343-356). CRC Press
Open this publication in new window or tab >>Multi-species multicellular life cycles
2022 (English)In: The evolution of multicellularity, CRC Press, 2022, p. 343-356Chapter in book (Refereed)
Abstract [en]

Textbook examples of multicellular organisms vary in their scale and complexity but are typically composed of a single species. The prevalence of entities such as lichens, however, suggest that two different species may be capable of forming a type of multi-species multicellularity-though it may not resemble its clonal counterparts. In this chapter, we consider the possibility of multi-species multicellularity and in particular its origins. Drawing upon previous studies of the evolutionary origins of clonal multicellularity, we focus on the emergence of simple reproducing groups that have the capacity to gain adaptations. We present a framework for organizing these initial multi-species group life cycles based on whether the constituent species are unicellular or multicellular and whether the groups reproduce via fragmentation or cycles of dissociation and re-association. We discuss characteristics of each type of multi-species multicellularity and representative examples to assess their likely evolutionary trajectories. Ultimately, we conclude that the multi-species groups that most resemble textbook multicellular organisms are composed of unicellular and multicellular species and reproduce via cycles of dissociation and re-association.

Place, publisher, year, edition, pages
CRC Press, 2022
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-200677 (URN)10.1201/9780429351907-21 (DOI)2-s2.0-85140170685 (Scopus ID)9781000542554 (ISBN)9780367356965 (ISBN)
Available from: 2022-11-01 Created: 2022-11-01 Last updated: 2024-05-20Bibliographically approved
Libby, E. & Ratcliff, W. C. (2021). Lichens and microbial syntrophies offer models for an interdependent route to multicellularity. The Lichenologist, 53(4), 283-290
Open this publication in new window or tab >>Lichens and microbial syntrophies offer models for an interdependent route to multicellularity
2021 (English)In: The Lichenologist, ISSN 0024-2829, E-ISSN 1096-1135, Vol. 53, no 4, p. 283-290Article, review/survey (Refereed) Published
Abstract [en]

The evolution of multicellularity paved the way for significant increases in biological complexity. Although multicellularity has evolved many times independently, we know relatively little about its origins. Directed evolution is a promising approach to studying early steps in this major transition, but current experimental systems have examined only a subset of the possible evolutionary routes to multicellularity. Here we consider egalitarian routes to multicellularity, in which unrelated unicellular organisms evolve to become a multicellular organism. Inspired by microbial syntrophies and lichens, we outline three such routes from a system of different species to an interdependent relationship that replicates. We compare these routes to contemporary experimental systems and consider how physical structure, the threat of invasion, division of labour and co-transmission affect their evolution.

Place, publisher, year, edition, pages
Cambridge University Press, 2021
Keywords
division of labour, experimental evolution, major transitions, microbes, multicellularity, syntrophy
National Category
Evolutionary Biology Other Mathematics
Identifiers
urn:nbn:se:umu:diva-186788 (URN)10.1017/S0024282921000256 (DOI)000679329600003 ()2-s2.0-85112055101 (Scopus ID)
Available from: 2021-08-24 Created: 2021-08-24 Last updated: 2021-08-24Bibliographically approved
Bozdag, G. O., Libby, E., Pineau, R., Reinhard, C. T. & Ratcliff, W. C. (2021). Oxygen suppression of macroscopic multicellularity. Nature Communications, 12(1), Article ID 2838.
Open this publication in new window or tab >>Oxygen suppression of macroscopic multicellularity
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2021 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 12, no 1, article id 2838Article in journal (Refereed) Published
Abstract [en]

Atmospheric oxygen is thought to have played a vital role in the evolution of large, complex multicellular organisms. Challenging the prevailing theory, we show that the transition from an anaerobic to an aerobic world can strongly suppress the evolution of macroscopic multicellularity. Here we select for increased size in multicellular ‘snowflake’ yeast across a range of metabolically-available O2 levels. While yeast under anaerobic and high-O2 conditions evolved to be considerably larger, intermediate O2 constrained the evolution of large size. Through sequencing and synthetic strain construction, we confirm that this is due to O2-mediated divergent selection acting on organism size. We show via mathematical modeling that our results stem from nearly universal evolutionary and biophysical trade-offs, and thus should apply broadly. These results highlight the fact that oxygen is a double-edged sword: while it provides significant metabolic advantages, selection for efficient use of this resource may paradoxically suppress the evolution of macroscopic multicellular organisms.

Place, publisher, year, edition, pages
Nature Publishing Group, 2021
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-186161 (URN)10.1038/s41467-021-23104-0 (DOI)000658733500006 ()33990594 (PubMedID)2-s2.0-85105925015 (Scopus ID)
Available from: 2021-07-15 Created: 2021-07-15 Last updated: 2023-03-28Bibliographically approved
Isaksson, H., Conlin, P. L., Kerr, B., Ratcliff, W. C. & Libby, E. (2021). The consequences of budding versus binary fission on adaptation and aging in primitive multicellularity. Genes, 12(5), Article ID 661.
Open this publication in new window or tab >>The consequences of budding versus binary fission on adaptation and aging in primitive multicellularity
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2021 (English)In: Genes, ISSN 2073-4425, E-ISSN 2073-4425, Vol. 12, no 5, article id 661Article in journal (Refereed) Published
Abstract [en]

Early multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells, whether they reproduce via binary fission or budding, can affect the rate of adaptation in primitive multicellularity. We use mathematical models to study the spread of beneficial, growth rate mutations in unicellular populations and populations of multicellular filaments reproducing via binary fission or budding. Comparing populations once they reach carrying capacity, we find that the spread of mutations in multicellular budding populations is qualitatively distinct from the other populations and in general slower. Since budding and binary fission distribute age-accumulated damage differently, we consider the effects of cellular senescence. When growth rate decreases with cell age, we find that beneficial mutations can spread significantly faster in a multicellular budding population than its corresponding unicellular population or a population reproducing via binary fission. Our results demonstrate that basic aspects of the cell cycle can give rise to different rates of adaptation in multicellular organisms.

Place, publisher, year, edition, pages
MDPI, 2021
Keywords
Adaptation, Aging, Binary fission, Budding, Filaments, Multicellularity
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-183525 (URN)10.3390/genes12050661 (DOI)000653921500001 ()2-s2.0-85105195781 (Scopus ID)
Available from: 2021-05-25 Created: 2021-05-25 Last updated: 2024-05-20Bibliographically approved
Smith, H. H., Hyde, A. S., Simkus, D. N., Libby, E., Maurer, S. E., Graham, H. V., . . . Johnson, S. S. (2021). The grayness of the origin of life. Life, 11(6), Article ID 498.
Open this publication in new window or tab >>The grayness of the origin of life
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2021 (English)In: Life, E-ISSN 2075-1729, Vol. 11, no 6, article id 498Article in journal (Refereed) Published
Abstract [en]

In the search for life beyond Earth, distinguishing the living from the non-living is paramount. However, this distinction is often elusive, as the origin of life is likely a stepwise evolutionary process, not a singular event. Regardless of the favored origin of life model, an inherent “grayness” blurs the theorized threshold defining life. Here, we explore the ambiguities between the biotic and the abiotic at the origin of life. The role of grayness extends into later transitions as well. By recognizing the limitations posed by grayness, life detection researchers will be better able to develop methods sensitive to prebiotic chemical systems and life with alternative biochemistries.

Keywords
Agnostic biosignatures, Evolutionary transitions, Lipids, Metalloenzymes, Meteoritic organics, Origin of life, Pre-RNAs, Prebiotic evolution, Thioesters
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-186359 (URN)10.3390/life11060498 (DOI)000666537400001 ()34072344 (PubMedID)2-s2.0-85107897069 (Scopus ID)
Available from: 2021-07-23 Created: 2021-07-23 Last updated: 2021-07-23Bibliographically approved
Projects
The Origin of the Eukaryotic Endosymbiosis: A theoretical framework for assessing the likelihood and impact of the mitochondrion [2018-03630_VR]; Umeå University
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-6569-5793

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