Evolution: To plasticity and back again
It was the Danish botanist Wilhelm Johannsen who coined the terms ‘genotype’ and ‘phenotype’. He thought that the genotype, or genetic makeup, of an organism referred to its ‘fundamental constitution’, whereas an organism's individual characters or traits, i.e. its phenotype, arose from a complicated interaction between the genotype and the environment (Johannsen, 1913).
Phenotypes can vary in response to external factors such as nutrition and temperature (Woltereck, 1909); this can be simply an accidental consequence of the fact that cellular and developmental processes that produce the phenotype run at different rates under different environmental conditions. And because environments are seldom, if ever, stable, it is very common for there to be some natural variation in phenotypes around some ‘ideal’ value, even between individuals with identical genotypes.
A natural question to ask is—does this variation matter? In terms of evolution, what matters are things that affect fitness: that is, things that affect the ability of an individual, compared to other individuals, to pass its genes to the next generation. If the phenotypic variation reduces fitness, then selection will favor the evolution of mechanisms that make the phenotype more robust, or less sensitive to environmental variation. On the other hand, if some of the phenotypes are well adapted to the environmental factors that induce them, evolution will favor mechanisms that stabilize the production of each phenotype in its best-suited environment.
When one genotype can produce more than one phenotype in different environments, this is generally referred to as ‘phenotypic plasticity’. As this ability can increase the diversity of phenotypes in a population, it is natural to ask whether populations of organisms with phenotypic plasticity are more able to evolve than those without. To date, there are various theories that suggest they should be, but there is little experimental evidence to support this view (Moczek et al., 2011; West-Eberhard, 2003). Now, in eLife, Ralf Sommer and Erik Ragsdale from the Max Planck Institute for Developmental Biology and co-workers—including Vladislav Susoy as first author—report that phenotypic plasticity is associated with evolutionary diversification in nematode worms (Susoy et al., 2015).
Susoy et al. examined a large group of nematode worms, including the model species Caenorhabditis elegans and some species with adults that have so-called ‘polyphenic’ mouthparts. Polyphenism is an extreme, but common, form of phenotypic plasticity in which two (or more) completely different phenotypes develop in response to specific environmental cues. Each of the alternative phenotypes is an adaptation to a different environment (Nijhout, 2003), and natural selection acts to ensure that they are stably and reliably produced to best match the environmental conditions.
Susoy et al. tested 90 species of nematodes for their ability to develop polyphenic mouthparts in the laboratory. In 23 species, some worms developed small smooth mouths specialized for feeding on bacteria, whereas others of the same species developed mouths with hooks and teeth. The toothed phenotype is used to feed on fungi and on other nematodes, and is induced by overcrowding and by starvation during the first larval stage (Bento et al., 2010; Sommer and Ogawa, 2011).
Analysis of the evolutionary relationships between the nematodes revealed that polyphenic mouthparts evolved only once in a common ancestor of the 23 species. Susoy et al. then asked if there was greater diversification in the shapes of mouthparts after polyphenism had evolved compared to the lineages of the ‘nematode family tree’ that had not evolved polyphenism. A sophisticated statistical analysis showed that this was indeed the case. This is some of the best empirical evidence to date for the theory that phenotypic plasticity enhances the ability of a population to evolve new forms (also known as evolvability).
Moreover, although polyphenism evolved only once, it appears to have been lost at least 10 times during the subsequent evolution of the lineage. Unexpectedly, the loss of polyphenism was followed by an even stronger rate of subsequent evolution of new traits and phenotypes. Thus the loss of phenotypic plasticity was also associated with an increase in evolvability. But how can this be explained?
One possible explanation is that a polyphenism requires developmental mechanisms that stabilize two alternative phenotypes, each in a different environment. If they work well, such stabilizing mechanisms buffer the two phenotypes against moderate changes to the organism's genetic makeup. This means that many mutations will not effect the phenotype and therefore will not be selected against. Such mutations will gradually accumulate in a population (Figure 1). Then, when the polyphenism is lost, the need to stabilize one of the two phenotypes disappears. Thus some of the accumulated genetic variation is no longer buffered and can cause the phenotype to vary more. This new phenotypic variation can now come under selection and lead to diverse adaptations in different lineages.
It is important to note that this explanation is, of course, a thought experiment that could be supported by statistical analyses. But the great challenge for the future will be to establish whether it is possible to devise experiments that can prove whether such a mechanism exists in nature.
References
-
The role of developmental plasticity in evolutionary innovationProceedings of the Royal Society B: Biological Sciences 278:2705–2713.https://doi.org/10.1098/rspb.2011.0971
-
Development and evolution of adaptive polyphenismsEvolution & Development 5:9–18.https://doi.org/10.1046/j.1525-142X.2003.03003.x
-
Weitere experimentelle Untersuchungen über Artveränderung, speziell über das Wesen quantitativer Artunterschiede bei DaphnienVerhandlungen der Deutschen Zoologischen Gesellschaft 19:110–173.
Article and author information
Author details
Publication history
- Version of Record published: March 12, 2015 (version 1)
Copyright
© 2015, Nijhout
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,651
- views
-
- 250
- downloads
-
- 8
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Computational and Systems Biology
- Evolutionary Biology
As the genome encodes the information crucial for cell growth, a sizeable genomic deficiency often causes a significant decrease in growth fitness. Whether and how the decreased growth fitness caused by genome reduction could be compensated by evolution was investigated here. Experimental evolution with an Escherichia coli strain carrying a reduced genome was conducted in multiple lineages for approximately 1000 generations. The growth rate, which largely declined due to genome reduction, was considerably recovered, associated with the improved carrying capacity. Genome mutations accumulated during evolution were significantly varied across the evolutionary lineages and were randomly localized on the reduced genome. Transcriptome reorganization showed a common evolutionary direction and conserved the chromosomal periodicity, regardless of highly diversified gene categories, regulons, and pathways enriched in the differentially expressed genes. Genome mutations and transcriptome reorganization caused by evolution, which were found to be dissimilar to those caused by genome reduction, must have followed divergent mechanisms in individual evolutionary lineages. Gene network reconstruction successfully identified three gene modules functionally differentiated, which were responsible for the evolutionary changes of the reduced genome in growth fitness, genome mutation, and gene expression, respectively. The diversity in evolutionary approaches improved the growth fitness associated with the homeostatic transcriptome architecture as if the evolutionary compensation for genome reduction was like all roads leading to Rome.
-
- Evolutionary Biology
Enantiornithines were the dominant birds of the Mesozoic, but understanding of their diet is still tenuous. We introduce new data on the enantiornithine family Bohaiornithidae, famous for their large size and powerfully built teeth and claws. In tandem with previously published data, we comment on the breadth of enantiornithine ecology and potential patterns in which it evolved. Body mass, jaw mechanical advantage, finite element analysis of the jaw, and traditional morphometrics of the claws and skull are compared between bohaiornithids and living birds. We find bohaiornithids to be more ecologically diverse than any other enantiornithine family: Bohaiornis and Parabohaiornis are similar to living plant-eating birds; Longusunguis resembles raptorial carnivores; Zhouornis is similar to both fruit-eating birds and generalist feeders; and Shenqiornis and Sulcavis plausibly ate fish, plants, or a mix of both. We predict the ancestral enantiornithine bird to have been a generalist which ate a wide variety of foods. However, more quantitative data from across the enantiornithine tree is needed to refine this prediction. By the Early Cretaceous, enantiornithine birds had diversified into a variety of ecological niches like crown birds after the K-Pg extinction, adding to the evidence that traits unique to crown birds cannot completely explain their ecological success.