Trends in Genetics
Volume 20, Issue 5, 1 May 2004, Pages 268-276
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Phenotypic neighborhood and micro-evolvability

https://doi.org/10.1016/j.tig.2004.03.010Get rights and content

Abstract

The complex relationship between the genotype and the phenotype constrains and biases phenotypic evolution. Indeed, random mutation can have non-random (anisotropic) effects on the phenotype. In this review, we propose an operational definition of the ‘phenotypic neighborhood’ of a given genotype, as obtained after induced mutagenesis or in mutation accumulation lines, with examples of anisotropic distributions of phenotypes reached when exploring the vicinity of a genotype. We also compare the phenotypic neighborhood for a given developmental process among species, focusing on nematode vulva development. Finally, we compare the phenotypic neighborhood assessed by mutagenesis with the phenotypic spectrum of wild isolates of the same species and make inferences about the action of selection and/or drift on the same developmental process in the wild.

Section snippets

Anisotropy in phenotypic mutability: Caenorhabditis elegans body size

Let us start with the example of a one-dimensional quantitative phenotype, that of body size (note that simplicity in the measure of the output does not imply that underlying mechanisms are simple). In C. elegans, three methods have been used to probe the mutability of body size: (i) genetic screens; (i) mutation accumulation lines; and (iii) selection in the laboratory (Box 2).

The starting genotype is that of the C. elegans reference strain N2 (an isogenic selfing strain). First, after induced

The phenotypic space of nematode vulva development

Let us now turn to a phenotype with more than one quantitative outcome, nematode vulva development, which provides a good system for such studies because its phenotypic space can be described by cell-level analysis and compared between species.

The vulva is the egg-laying organ of female and hermaphrodite nematodes. It develops from the same ventral epidermal Pn.p cells in different nematode species (Pn.p cells are numbered 1–12 from the anterior to the posterior of the animal). In C. elegans,

Parallel mutageneses for vulva development in different nematode species

Strikingly, the number of genetic loci that are recovered for each of the three steps of vulva formation differs among the species (Figure 2). O. tipulae seems to mutate easily for the Pn.p division step and poorly for the vulval-fate-specification mechanisms. By contrast, in C. elegans it is easy to obtain mutants that affect Pn.p specification but not their divisions per se. In other words, the mutational variance is high for some developmental traits in one species and low for another.

Consequences on evolvability: the ‘phenotypic neighborhood’

Each species (or more precisely each genotype) thus has a specific mutational profile for a given biological process. We use the term ‘phenotypic neighborhood’ as an operational definition of phenotypic evolvability, based on the spectrum and the density of phenotypes obtained when a given genotype is systematically mutated, either by induced or by spontaneous mutagenesis, irrespective of its selective value in wild populations. ‘Neighborhood’ is meant to indicate that the relevant genotype is

Mutational variability compared with natural variation

The examples discussed previously explore the capacity to evolve new phenotypes without selection (other than requiring survival). This evolvability can then be compared with the result of evolution in the wild, after the action of natural sorting (selection and random drift), and the effect of natural selection thus inferred. Assuming that all phenotypes obtained in the laboratory can be reached by random mutation in large wild populations, then the phenotypes obtained in the laboratory and

A micro-evolutionary evolvability

This leads us to the last question: does the phenotypic neighborhood reflect long-term evolution of a group of organisms? Finding wild variants that resemble laboratory mutants or, conversely, finding ‘atavistic’ mutations, has a long and controversial history. For example, the Drosophila four-wing mutations [43] could have reflected the genetic change corresponding to the development of four wings in other insect orders but they did not [44]. However, at a smaller evolutionary timescale,

Concluding remarks

Evolution is the product of evolvability followed by sorting in wild populations. ‘Classical genetics’ studies can be used to answer evolutionary questions concerning phenotypic evolvability in complex genotype-to-phenotype mapping and to compare relative phenotypic distributions of laboratory mutants with wild variants at a micro-evolutionary timescale. A strikingly distinct spectrum of vulva phenotypes was obtained in three nematode species. For some traits, the variation correlates with wild

Acknowledgements

We are grateful to our many colleagues for helpful discussions. We thank Jean Deutsch, Greg Gibson, Michel Labouesse, Eli Meir and the reviewers for their comments. Many thanks to Michael Lynch and members of his laboratory for the C. elegans mutation accumulation lines and to Ralf Sommer and his laboratory for communication of unpublished results. Our work is supported by grants from CNRS, ARC, Ministry of Research (France) and HFSP.

Glossary

Glossary

Evolvability:
the capacity to evolve at the phenotypic level, irrespective of the action of natural selection. This term has been used to underline the great capacity of biological systems to evolve [55] or their ability to respond to selection [11]. We employ the word ‘capacity’ (as, for example, in ‘electrical capacity’ or ‘visibility’) in a more neutral manner and do not imply that it is either high or adaptive.
Phenotypic neighborhood:
the range and distribution of phenotypes that are reached

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