Continual evolution through coupled fast and slow feedbacks

AbstractThe Red Queen Hypothesis, which suggests that continual evolution can result from solely biotic interactions, has been studied in macroevolutionary and microevolutionary contexts. While microevolutionary studies have described examples in which evolution does not cease, understanding which general conditions lead to continual evolution or to stasis remains a major challenge. In many cases, it is unclear which experimental features or model assumptions are necessary for the observed continual evolution to emerge, and whether the described behavior is robust to variations in the given setup. Here, we aim to find the minimal set of conditions under which continual evolution occurs. To this end, we present a theoretical framework that does not assume any specific functional form and, therefore, can be applied to a wide variety of systems. Our framework is also general enough to cast predictions about both monomorphic and polymorphic populations. We show that the combination of a fast positive and a slow negative feedback causes continual evolution to emerge even from the evolution of one single evolving trait, provided that the ecological timescale is sufficiently separated from the timescales of mutation and the negative feedback. Our approach and results thus contribute to a deeper understanding of the evolutionary dynamics resulting from biotic interactions.

Download Full-text

Continual evolution through coupled fast and slow feedbacks

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1916345117 ◽

2020 ◽

Vol 117 (8) ◽

pp. 4234-4242 ◽

Cited By ~ 1

Author(s):

Meike T. Wortel ◽

Han Peters ◽

Juan A. Bonachela ◽

Nils Chr. Stenseth

Keyword(s):

Negative Feedback ◽

Evolutionary Dynamics ◽

Functional Form ◽

Biotic Interactions ◽

Theoretical Framework ◽

Red Queen Hypothesis ◽

Red Queen ◽

Minimal Set ◽

The Given ◽

The Red Queen

Continual evolution describes the unceasing evolution of at least one trait involving at least one organism. The Red Queen Hypothesis is a specific case in which continual evolution results from coevolution of at least two species. While microevolutionary studies have described examples in which evolution does not cease, understanding which general conditions lead to continual evolution or to stasis remains a major challenge. In many cases, it is unclear which experimental features or model assumptions are necessary for the observed continual evolution to emerge, and whether the described behavior is robust to variations in the given setup. Here, we aim to find the minimal set of conditions under which continual evolution occurs. To this end, we present a theoretical framework that does not assume any specific functional form and, therefore, can be applied to a wide variety of systems. Our framework is also general enough to make predictions about both monomorphic and polymorphic populations. We show that the combination of a fast positive and a slow negative feedback between environment, population, and evolving traits causes continual evolution to emerge even from the evolution of a single evolving trait, provided that the ecological timescale is sufficiently faster than the timescales of mutation and the negative feedback. Our approach and results thus contribute to a deeper understanding of the evolutionary dynamics resulting from biotic interactions.

Download Full-text

The evolutionary significance of mass extinctions

Catastrophes and Lesser Calamities ◽

10.1093/oso/9780198524977.003.0013 ◽

2004 ◽

Author(s):

Tony Hallam

Keyword(s):

Biotic Interactions ◽

Evolutionary Significance ◽

Red Queen Hypothesis ◽

Mass Extinctions ◽

Red Queen ◽

Physical Conditions ◽

The Face ◽

Competition For Food ◽

Zero Sum ◽

The Red Queen

Darwin was firmly of the opinion that biotic interactions, such as competition for food and space – the ‘struggle for existence’ – were of considerably greater importance in promoting evolution and extinction than changes in the physical environment. This is clearly brought out by this quotation from The Origin of Species: . . . Species are produced and exterminated by slowly acting causes . . . and the most important of all causes of organic change is one that is almost independent of altered . . . physical conditions, namely the mutual relation of organism to organism – the improvement of one organism entailing the improvement or extermination of others. . . . The driving force of competition in a crowded world is also stressed in another quotation presenting Darwin’s famous wedge metaphor: . . . In looking at Nature, it is most necessary . . . never to forget that every single organic being around us may be said to be striving to the utmost to increase in numbers; that each lives by a struggle at some period of its life; that heavy destruction inevitably falls either on the young or the old, during each generation . . . The face of Nature may be compared to a yielding surface, with ten thousand sharp wedges packed close together and driven inwards by incessant blows, sometimes one wedge being struck, and then another with greater force. . . . The implication of the Darwinian view concerning the dominance of biotic competition is that for each winner there is a loser – a kind of zero-sum game. It has been accepted more or less uncritically by generations of evolutionary biologists, but not until the 1970s did it become graced with a name – the Red Queen hypothesis. The story behind the emergence of this name is an interesting one. At the beginning of the 1970s the rather eccentric University of Chicago palaeobiologist Leigh Van Valen did some interesting research concerning the analysis of survivors of Phanerozoic taxa which suggested that the probability of a fossil group becoming extinct was more or less constant in time. To account for this, Van Valen put forward his Red Queen hypothesis.

Download Full-text

Getting somewhere with the Red Queen: chasing a biologically modern definition of the hypothesis

Biology Letters ◽

10.1098/rsbl.2017.0734 ◽

2018 ◽

Vol 14 (5) ◽

pp. 20170734 ◽

Cited By ~ 14

Author(s):

Luke C. Strotz ◽

Marianna Simões ◽

Matthew G. Girard ◽

Laura Breitkreuz ◽

Julien Kimmig ◽

...

Keyword(s):

Conceptual Understanding ◽

Biotic Interactions ◽

Population Level ◽

Red Queen Hypothesis ◽

Red Queen ◽

Evolutionary Patterns ◽

Evolutionary Theories ◽

Definition Of ◽

The Red Queen

The Red Queen hypothesis (RQH) is both familiar and murky, with a scope and range that has broadened beyond its original focus. Although originally developed in the palaeontological arena, it now encompasses many evolutionary theories that champion biotic interactions as significant mechanisms for evolutionary change. As such it de-emphasizes the important role of abiotic drivers in evolution, even though such a role is frequently posited to be pivotal. Concomitant with this shift in focus, several studies challenged the validity of the RQH and downplayed its propriety. Herein, we examine in detail the assumptions that underpin the RQH in the hopes of furthering conceptual understanding and promoting appropriate application of the hypothesis. We identify issues and inconsistencies with the assumptions of the RQH, and propose a redefinition where the Red Queen's reign is restricted to certain types of biotic interactions and evolutionary patterns occurring at the population level.

Download Full-text

Evidence of the Red-Queen Hypothesis from Accelerated Rates of Evolution of Genes Involved in Biotic Interactions in Pneumocystis

Genome Biology and Evolution ◽

10.1093/gbe/evy116 ◽

2018 ◽

Vol 10 (6) ◽

pp. 1596-1606 ◽

Cited By ~ 4

Author(s):

Luis Delaye ◽

Susana Ruiz-Ruiz ◽

Enrique Calderon ◽

Sonia Tarazona ◽

Ana Conesa ◽

...

Keyword(s):

Biotic Interactions ◽

Red Queen Hypothesis ◽

Red Queen ◽

Rates Of Evolution ◽

The Red Queen

Download Full-text

THE RED QUEEN HYPOTHESIS AND PLANT/PATHOGEN INTERACTIONS

Annual Review of Phytopathology ◽

10.1146/annurev.phyto.34.1.29 ◽

1996 ◽

Vol 34 (1) ◽

pp. 29-50 ◽

Cited By ~ 129

Author(s):

Keith Clay ◽

Paula X. Kover

Keyword(s):

Plant Pathogen ◽

Red Queen Hypothesis ◽

Red Queen ◽

Plant Pathogen Interactions ◽

The Red Queen

Download Full-text

The Red Queen model of recombination hot-spot evolution: a theoretical investigation

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0463 ◽

2017 ◽

Vol 372 (1736) ◽

pp. 20160463 ◽

Cited By ~ 14

Author(s):

Thibault Latrille ◽

Laurent Duret ◽

Nicolas Lartillot

Keyword(s):

Gene Conversion ◽

Recombination Rate ◽

Evolutionary Dynamics ◽

Genetic Model ◽

Hot Spot ◽

Rate Variation ◽

Red Queen ◽

Biased Gene Conversion ◽

Red Queen Model ◽

The Red Queen

In humans and many other species, recombination events cluster in narrow and short-lived hot spots distributed across the genome, whose location is determined by the Zn-finger protein PRDM9. To explain these fast evolutionary dynamics, an intra-genomic Red Queen model has been proposed, based on the interplay between two antagonistic forces: biased gene conversion, mediated by double-strand breaks, resulting in hot-spot extinction, followed by positive selection favouring new PRDM9 alleles recognizing new sequence motifs. Thus far, however, this Red Queen model has not been formalized as a quantitative population-genetic model, fully accounting for the intricate interplay between biased gene conversion, mutation, selection, demography and genetic diversity at the PRDM9 locus. Here, we explore the population genetics of the Red Queen model of recombination. A Wright–Fisher simulator was implemented, allowing exploration of the behaviour of the model (mean equilibrium recombination rate, diversity at the PRDM9 locus or turnover rate) as a function of the parameters (effective population size, mutation and erosion rates). In a second step, analytical results based on self-consistent mean-field approximations were derived, reproducing the scaling relations observed in the simulations. Empirical fit of the model to current data from the mouse suggests both a high mutation rate at PRDM9 and strong biased gene conversion on its targets. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

Download Full-text