Elsevier

Biosystems

Volume 69, Issues 2–3, May 2003, Pages 163-185
Biosystems

Prokaryote and eukaryote evolvability

https://doi.org/10.1016/S0303-2647(02)00131-4Get rights and content

Abstract

The concept of evolvability covers a broad spectrum of, often contradictory, ideas. At one end of the spectrum it is equivalent to the statement that evolution is possible, at the other end are untestable post hoc explanations, such as the suggestion that current evolutionary theory cannot explain the evolution of evolvability. We examine similarities and differences in eukaryote and prokaryote evolvability, and look for explanations that are compatible with a wide range of observations. Differences in genome organisation between eukaryotes and prokaryotes meets this criterion. The single origin of replication in prokaryote chromosomes (versus multiple origins in eukaryotes) accounts for many differences because the time to replicate a prokaryote genome limits its size (and the accumulation of junk DNA). Both prokaryotes and eukaryotes appear to switch from genetic stability to genetic change in response to stress. We examine a range of stress responses, and discuss how these impact on evolvability, particularly in unicellular organisms versus complex multicellular ones. Evolvability is also limited by environmental interactions (including competition) and we describe a model that places limits on potential evolvability. Examples are given of its application to predator competition and limits to lateral gene transfer. We suggest that unicellular organisms evolve largely through a process of metabolic change, resulting in biochemical diversity. Multicellular organisms evolve largely through morphological changes, not through extensive changes to cellular biochemistry.

Introduction

Evolvability is a central concept in evolution but is easily misconstrued, hence its use must be defined carefully. At a basic level, evolvability is the fundamental concept of evolution. From the late-17th to mid-19th centuries it was generally assumed that species had an unchangeable ‘essence’. This Platonic concept was introduced in the late-17th century when it became increasingly clear that continuing spontaneous generation of larger life forms did not occur (see Farley, 1977). If species had an unchangeable essence then, by definition, there could be no evolution, even if individual organisms deviated from the ‘ideal type’. ‘Evolvability’, by denying species have an unchangeable essence, is central to evolution. Since all evolutionists agree, this definition is not that interesting.

Burch and Chao (2000) offer a more limited definition, “the ability to generate adaptive mutations”. We consider the two aspects of this definition: ‘adaptive mutations’ and ‘ability to generate’. That adaptive mutations occur is the evolvability concept from the previous paragraph, but in modern terminology: some mutations are advantageous. In the early 19th century many accepted selection, but only in elimination of deleterious variants. Selection, by eliminating such variants, tended to preserve the unchanging essence of the species. In contrast, the existence of adaptive variants and positive selection allows evolution through time and is an essential part of evolvability.

The ‘ability to generate’ adaptive mutations is more problematic, and is mirrored in Kirschner and Gerhart’s (1998) definition: ‘the capacity to generate (our emphasis) heritable, selectable phenotypic variation’. If it is simply the observation that advantageous mutations occur, then, again, the usage is uncontroversial, though uninteresting. If it implies that advantageous mutations can be generated ‘on demand’ (e.g. Cairns et al., 1988) then it is a specialised (and controversial) usage. Some discussions on evolvability appear to give the impression of ‘the more change the better’—yet most major change is highly deleterious. For instance, Radman et al. (1999) point out that selection for increased fidelity of DNA synthesis has been achieved with Escherichia coli in the laboratory (Fijalkowska et al., 1993), and that this demonstrates ‘there was no durable selective pressure in nature for maximal fidelity’.

However, the majority of discussions on evolvability (e.g. Wagner and Altenberg, 1996, Wagner, 1996, Kirschner and Gerhart, 1998, Partridge and Barton, 2000), acknowledge directed mutation is not required to understand evolvability. Nevertheless, confusion arises easily, as shown by reactions to work from Lindquist’s group (Rutherford and Lindquist, 1998, True and Lindquist, 2000). Other workers (Dickinson and Seger, 1999, Partridge and Barton, 2000) concluded that these authors favoured the idea that certain traits have been selected for their utility to contribute to organismal evolvability, and nothing else. While Lindquist points out that this was never her interpretation (Lindquist, 2000), the subsequent correspondence generated by this work (Dickinson and Seger, 1999, Partridge and Barton, 2000, Dover, 2000) illustrates how problematic this concept can be. There is no agreed definition for evolvability that explicitly avoids the problem of evolutionary forethought. Indeed, whenever the phrase ‘the evolution of evolvability’ is used, there is the possibility of it being misconstrued. This is not because evolvability cannot evolve through accepted processes of evolution. Rather, under known processes of Darwinian evolution, evolvability cannot evolve in itself because the origin and maintenance of a trait would have to precede selection for the trait.

Evolvability can be a by-product of selection however. For example, activation of a transposable element might lead to a mutation that is selected, thereby inadvertently leading to additional mutations (through additional element insertions) in the future. Such future mutations may be deleterious or advantageous; the increased mutation rate is a by-product of the transposable element hitchhiking with the selected mutation.

Still at issue is the evolutionary origin of traits that contribute to evolvability and adaptive mutations. Examination of the origins of such traits is an important step in alleviating controversy surrounding this area. This is particularly so with evolvability in multicellular organisms, where one gets the impression that we should be in awe of the exciting molecular and genetic mechanisms that contribute to eukaryote evolvability (Kirschner and Gerhart, 1998, Herbert and Rich, 1999). Other reviews on the evolution of evolvability (e.g. Partridge and Barton, 2000, Kirschner and Gerhart, 1998, Moxon and Thaler, 1997) identify mechanisms by which genome architecture can influence this (see also Table 2).

This paper is divided into sections that discuss the following topics:

  • Section 2: Selection versus neutral evolution.

  • Section 3: Parasites: evolvability or reductive evolution?

  • Section 4: Consequences of prokaryote and eukaryote genome architecture.

  • Section 5: The stress response and evolvability.

  • Section 6: An ecological perspective: evolutionarily-stable niche-discontinuity (ESND).

  • Section 7: Plasticity, learning and evolvability.

Briefly, Section 2 gives a theoretical frame of reference from which to consider the possibility that not all complex traits that impact on evolvability are necessarily a product of selection. In Section 3, we aim to emphasise that, despite parasitism having arisen multiple times in evolution, there was probably nothing about the ancestral groups from which various parasites emerged that made them inherently more ‘evolvable’. Rather, ecological limitations, and phenomena consequent to parasitism may better explain parasite evolution—parasites do not consititute a ‘special case’ with regards the ‘evolution of evolvability’. In Section 4 we consider the origins and impact of a range of phenomena that contribute to the genome architectures and gene expression systems of eukaryotes and prokaryotes (bacteria and archaea). We conclude that eukaryote architecture largely arose through neutral mechanisms, while reductive evolution was central to the emergence of prokaryote architecture. The consequences of these mechanisms for evolvability in prokaryotes and eukaryotes are discussed. In Section 5, the prokaryote–eukaryote division becomes blurred by considering the consequences of environmental stress for evolvability: constitutive multicellular eukaryotes with complex development are separated from ‘simple’ eukaryotes and prokaryotes. A contrast is drawn between periods where either genetic stability or change will be selectively advantageous. Experimental data, both with bacterial and metazoan models, point towards a general response to stress as being important in understanding how traits contributing to evolvability may have hitchhiked on survival of individuals. We focus on hypermutation (the elevation of mutation rate, either at a specific locus, or across the entire genome) and horizontal gene transfer (including meiotic recombination).

In Section 6 we discuss how the physical and biotic environment limits evolvability, allowing a distinction to be drawn between potential and realised evolvability (Fig. 2). Our model, which we call evolutionarily-stable niche-discontinuity (ESND), describes how competition allows colonisation of a fitness peak, and subsequently, how intraspecific competition limits movement away from that peak (Fig. 1). Examples of interspecies competition and predator–prey coevolution are considered, and are aimed at understanding evolvability in eukaryotes. The likely effects of horizontal gene transfer on ESNDs in bacteria are also considered.

Finally, we briefly consider phenotypic plasticity in eukaryotes. We are not aware of clear examples of non-genetic components to phenotypic plasticity in prokaryotes. However, ‘social behaviour’ and the emergence of phenotype switching in bacteria may be interesting in this regard.

Section snippets

Selection versus neutral evolution

There are strong parallels in the evolution of complexity and the evolution of evolvability. Neither complexity nor evolvability can be directly selected for; both impact future evolution, and hence are in violation of evolution as tinkering. Szathmáry and Maynard Smith (1995) point out that ‘There is no theoretical reason to expect evolutionary lineages to increase in complexity with time, and no empirical evidence that they do so’. Unlike with evolvability however, there is little apparent

Parasites: evolvability or reductive evolution?

Parasites are interesting in regard to evolvability because they represent a strategy common to eukaryotes, prokaryotes, viruses, and selfish elements. Parasites are often fast-evolving, and the move from a non-parasitic to a parasitic lifestyle has occurred frequently. We consider the following questions:

  • Were ancestral groups from which parasites arose inherently more ‘evolvable’?

  • If there is fast evolution in parasites, are they inherently more evolvable?

  • Is the concept of evolvability useful

Consequences of prokaryote and eukaryote genome architecture

In this section, we argue that many complexities of the eukaryote genome can be explained by the null hypothesis of neutralism, while the prokaryote genome cannot. It is almost universally assumed that eukaryotes evolved from ancestral prokaryote forms, an assumption that seems intuitively correct. However, it is just that—an intuitive bias that simple evolves to complex—and is taken as given by a large majority of researchers (see Forterre and Philippe, 1999 for critique). An extensive body of

The stress response and evolvability

In this section, we consider how stress responses promote organismal survival. Under some circumstances (see Table 1), hypermutation (adaptive evolution), horizontal transfer, sex in organisms with an asexual cycle, recombination, cell–cell interactions, and cell specialisation can all be understood as stress adaptations. That they contribute to evolvability in prokaryotes and unicellular organisms is consequential—these traits have not been selected for their propensity to promote

An ecological perspective: evolutionarily-stable niche-discontinuity (ESND)

Between groups of taxa (complex multicellular ones in particular), there often appear to be long-term stable niche boundaries. In a fitness landscape these boundaries limit access to a single peak, or subset of peaks, and thus limit evolutionary potential. For example, the vertebrate flying insectivore niche has been occupied by birds at day and bats at night for over 55 million years (Novacek, 1985) with little crossover between nocturnal and diurnal niches. Dinosaurs and mammals may have

Plasticity, learning and evolvability

Population genetics typically considers just the genetic contribution to the phenotype on the grounds that the genetic component is selectable. Phenotypic plasticity, such as the specific branching pattern of a tree that has grown into a gap of light in the forest, is not genetically determined—yet has an important bearing on evolvability. One suggestion, often called the Baldwin effect (Baldwin (1896), though also proposed by others), is that useful non-genetically acquired phenotypes will

Conclusions

In this paper, we have examined a wide range of biological phenomena relevant to the concept of evolvability. In agreement with most authors, we conclude that there is no need to explain evolvability as having evolved in itself; the evolution of phenomena contributing to evolvability can be explained by current evolutionary theory. It is important to base models for evolvability on a range of data, rather than establishing post hoc explanations for a single dataset. To this end, we have

Acknowledgements

We thank David Martin for helpful discussions and advice regarding the epigenotype concept, and two anonymous reviewers for helpful suggestions on how to improve the manuscript. This work was supported by the New Zealand Marsden Fund.

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