Held, Torsten ORCID: 0000-0002-1131-1950 (2018). Universality in the Evolution of Molecular Phenotypes. PhD thesis, Universität zu Köln.

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Abstract

With massive growth of biological sequence data and evolutionary experiments the quantitative modeling of evolutionary processes is made possible. These models aim to quantify the degree of conservation and the speed of adaptation in the evolution of biological systems. Evolutionary processes are driven by mutations, selection, and genetic drift. Mutations generate new variants, natural selection favors some of these, and genetic drift is the randomness in their reproduction success. In the early days of population genetics, it was identified that these processes can be described by employing mathematical models from statistical mechanics such as diffusion equations. Recent theoretical studies modeled and solved the dynamics for complex, interacting systems. The complexity arises through evolutionary interaction. On the one hand, mutations interact in their effect on selection. On the other hand, there is competing co-evolution of variants, if recombination cannot break up genomic links. Both problems arise naturally when considering the evolution of molecular phenotypes such as gene expression levels, protein stabilities, or biophysical binding properties. The inheritable information of these phenotypes is constituted by many sites of the DNA sequence. These sites give a large target to new mutational variants and, hence, a number of competing mutations. Since the sites are often confined to small regions of the DNA, beneficial variants in different individuals cannot be recombined through forms of horizontal gene transfer. Selection is further shaped by generically non-linear fitness landscapes, which is the mapping from the phenotypes to biological growth rates. Recent theoretical breakthroughs allowed for the description of the phenotypic dynamics decoupled from plenty of genomic details. These dynamics were solved in evolutionary equilibrium. In this thesis, we take up these models to describe various modes of their evolution, which are scenarios of time-dependent selection and in the co-evolution with other genes. We study for the first time the phenotypic evolution in time-dependent fitness landscapes, so called fitness seascapes, with underlying genomic sites that are genetically linked. We find universal properties that break down the relevant parameters to the stabilizing strength and the driving rate of the fitness seascape. These determine the divergence pattern on the phenotypic scale and the fitness flux, which is a measure for deviations from detailed balance and adaptation, on macro-evolutionary timescales. Therefore, we can read off the stabilizing strength and the fitness flux from the time-dependent phenotypic divergence/diversity ratio. Moreover, we study the impact of short-term constraining phenotypic selection on correlations in their constituting sequences. These correlations arise because sites compensate for the destructive effect from adaptation and genetic drift of other sites. We find that phenotypic evolution generates broad epistasis and correlation matrices across all trait sites, which are of low dimension. This kind of universality allows to read off from sequence correlations alone the number of traits under selection,the genotype–phenotype map, and single site adaptation. The latter can be identified from the asymmetry of time-ordered correlation measures, i.e. deviations from detailed balance. Furthermore, we join the dynamics with recent theories of asexual evolution. These showed universality in the scaling laws of fitness statistics under large mutational influx. With this, we make the step towards systems biology by studying for the first time the asexual co-evolution of biophysical phenotypes on a genome-wide level. We again find universality in the scaling of fitness statistics with the genome size, which decouples from the details of selection. This evolutionary mode induces a so far unknown and dramatic long-term cost of complexity, which can be overcome with small rates of horizontal gene transfer. Comparing this cost to actual biological genome sizes and recombination rates, this offers a new, feasible pathway for the evolution of sex. In all these modes we find so-far unknown laws of universality. These reduce the complexity of the processes on the higher level, e.g. the phenotypic or the overall fitness level and allow the inference of relevant parameters shaping the dynamics or to quantify scalings. Moreover, universalities are strongly related to the predictability of the evolutionary process.

Item Type: Thesis (PhD thesis)
Translated abstract:
AbstractLanguage
Die stark wachsende Anzahl biologischer Sequenzdaten und evolutionärer Experimente ermöglicht die quantitative Modellierung evolutionärer Prozesse. Diese Modelle zielen darauf ab, den Grad der Erhaltung und die Geschwindigkeit der Anpassung in der Evolution biologischer Systeme zu bestimmen. Der evolutionäre Prozess wird durch Mutationen, Selektion und genetischen Drift bestimmt. Mutationen erzeugen neue Variationen, natürliche Selektion bevorzugt einige hiervon, und genetischer Drift ist der Zufall im Reproduktionserfolg. Man hat früh erkannt, dass dieser Prozess durch den Einsatz von mathematischen Modellen aus der statistischen Physik, wie etwa Diffusionsgleichungen, beschrieben werden kann. Neuere theoretische Erkenntnisse erlauben die Modellierung der Dynamik komplexer, interagierender Systeme. Die Komplexität entsteht durch evolutionäre Interaktion. Einerseits interagieren Mutationen in ihren Fitnesseffekten. Andererseits existiert eine konkurrierende Koevolution verschiedener Varianten, wenn Rekombination die genomischen Verbindungen nicht aufbrechen kann. Beide Probleme treten auf, wenn man die Entwicklung molekularer Phänotypen wie Genexpressionslevels, Proteinstabilitäten oder biophysikalische Bindungseigenschaften betrachtet. Die vererbbare Information dieser Phänotypen besteht aus vielen Positionen der DNA-Sequenz. Diese geben ein großes Angriffsziel für neue Mutationsvarianten und damit eine Reihe von konkurrierenden Mutationen. Da sie oftmals auf kleine Bereiche der DNA beschränkt sind, können vorteilhafte Varianten bei verschiedenen Individuen nicht durch horizontalen Gentransfer rekombiniert werden. Die Selektion wird weiterhin generisch durch nichtlineare Fitnesslandschaften geprägt. Diese sind die Abbildung von den Phänotypen auf Wachstumsraten. Neuere theoretische Erkenntnisse erlauben es, diese phänotypische Dynamik losgelöst von vielen genomischen Details zu beschreiben. Hier greifen wir dies auf, um verschiedene Formen phänotypischer Evolution zu betrachten. Wir untersuchen zum ersten Mal die phänotypische Evolution in zeitabhängigen Fitnesslandschaften, so genannten Fitness-‘seascapes’, mit zugrunde liegenden genomischen Sequenzen, die genetisch zusammenhängend sind. Wir finden universelle Eigenschaften, welche die relevanten Parameter auf die Stärke stabilisierender Selektion und die zeitliche Änderungsrate der Fitness-‘seascape’ reduzieren. Diese bestimmen das Divergenzverhalten auf der phänotypischen Skala und den generierten Fitness Fluss, welcher die Abweichung vom detaillierten Gleichgewicht und die Stärke der Adaptation misst. Daher können die stabilisierende Selektion und die Adaptation vom zeitlich aufgelösten Divergenz-Diversitätsverhältnis bestimmt werden. Weiterhin untersuchen wir den Einfluss von stabilisierender phänotypischer Selektion auf die Korrelationen in diesen Sequenzen. Diese Korrelationen entstehen durch die Kompensation schadhafter Mutationen anderer DNA Positionen des Phänotypen, welche durch genetischen Drift oder Adaptation auftreten können. Wir lernen, dass phänotypische Evolution Epistasis und Korrelationengeneriert, die all diese Positionen umfassen. Nichtsdestotrotz sind diese von niedriger Dimension. Diese Universalität ermöglicht es von Sequenzkorrelation die Anzahl selektionsrelevanter Phänotypen, ihre Genotyp-Phänotyp-Abbildungen sowie Adaptation bestimmter Positionen zu erlernen. Letztere kann aus der Asymmetrie der zeitabhängigen Korrelationen identifiziert werden, welche Abweichungen des detaillierten Gleichgewichts messen. Schließlich begeben wir uns in die Systembiologie, indem wir erstmals die asexuelle Koevolution biophysikalischer Phänotypen auf genomweiter Ebene untersuchen. Wir finden universelle Skalierungsgesetze für die genomweite Fitnessstatistik, welche von Details der Selektion entkoppeln. Wir zeigen, dass diese zu dramatischen Kosten in der Genomgröße führen. Beim Vergleich unserer Ergebnisse mit realen biologischen Daten identifizieren wir einen neuen, selektiv praktikablen Weg für die Evolution zur Ausbildung der Geschlechter. In all diesen Modi finden wir Universalitäten. Diese reduzieren die Komplexität der Prozesse auf der höheren Ebene, z. B. der phänotypische Ebene oder der Gesamtfitness. Die Universalitäten erlauben die Inferenz relevanter Parameter, welche die Dynamik von Phänotypen beeinflussen, sowie die Identifizierung von Skalierungsgesetzen. Weiterhin stehen sie im engen Zusammenhang zur Vorhersagbarkeit des evolutionarären Prozesses.German
Creators:
CreatorsEmailORCID
Held, TorstenUNSPECIFIEDorcid.org/0000-0002-1131-1950
URN: urn:nbn:de:hbz:38-85500
Subjects: Natural sciences and mathematics
Physics
Life sciences
Uncontrolled Keywords:
KeywordsLanguage
Phenotypic Evolution; Population Genetics; Adaptive Evolution; Asexual Evolution; Evolution of Sex; BiophysicsEnglish
UNSPECIFIEDGerman
UNSPECIFIEDGerman
UNSPECIFIEDGerman
Faculty: Faculty of Mathematics and Natural Sciences
Divisions: Faculty of Mathematics and Natural Sciences > Department of Physics > Institute for Theoretical Physics
Language: English
Date: 2018
Date of oral exam: 19 July 2018
Referee:
NameAcademic Title
Lässig, MichaelProf. Dr.
Berg, JohannesProf. Dr.
Frey, ErwinProf. Dr.
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Refereed: Yes
URI: http://kups.ub.uni-koeln.de/id/eprint/8550

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