Evolution happens in populations, but the genetic changes that lead to adaptation arise and confer a benefit in individuals. Traditional evolutionary theory tells us a lot about how beneficial mutations spread through populations, but provides little insight into how such adaptive mutations arise in the first place. Modern concepts of evolvability try to capture both levels, relating the rate of adaptive evolution of a population to the properties of the genomes within that population.
Sometimes the rate of adaptation is a very conspicuous aspect of an organism, such as in pathogens that evolve resistance to treatment. But thinking about rates of adaptation turns out to be a pretty interesting way of looking at many questions all across the domains of life. Have a look at some examples below to get a sense of the diversity of ways that people are using evolvability to explore all sorts of mysteries in biology.
1. E. coli Subtle genetic changes potentiate a dramatic metabolic innovation.
Since 1988, Rich Lenski at MSU has been evolving twelve populations of E. coli in a relatively simple lab environment. These populations have experienced more than 50,000 generations in this constant, perhaps even boring, lab environment, yet their evolutionary dynamics continue to yield surprises. In 2008, Zachary Blount, Christina Borland, and Richard Lenski published a startling discovery–after over 30,000 generations in the presence of citrate, one population had suddenly evolved the ability to digest this potential nutrient. Replay experiments, in which frozen samples of the ancestors of this population are revived and allowed to evolve, showed that some mutations that had occurred 10,000 generations earlier must had been required for this innovation to evolve. A subsequent paper provided strong evidence for epistasis between these prerequisite mutations and the subsequent changes that directly caused the innovation, demonstrating how changes in evolvability–here seen as the rate at which adaptive mutations arise–may have their roots in more subtle genetic changes.
2. Poliovirus & Bacteriophage Phi-6 Synonymous sequences mutate & evolve differently
The genetic code seems completely understood and yet still a little mysterious–is it an arbitrary assignment of codes to amino acids, or a highly optimized arrangement? We quickly learn to call mutations that change the DNA sequence, but preserve the amino acids sequence, synonymous, but what does this really mean? “Synonyms” are similar but certainly not identical, and many biologists have noted that synonymous mutations may have interesting connections to adaptation.
One of my favorite recent demonstrations of the evolutionary significance of synonymous variants is a recent paper in Cell Host & Microbe by Adam Lauring, Ashley Acevedo, Samantha Cooper, and Raul Andino. This study used poliovirus, one of the best-studied models for virus replication, to see if changing the codons used to encode its capsid protein, without changing the protein sequence itself, would have any effect on the virus’s ability to adapt. An earlier study built synthetic versions of the capsid gene as negative controls for a study on codon usage, and so engineered massive shifts in the DNA sequence while preserving many subtle properties like overall codon frequency and RNA structure. Despite the similarities among these different encodings, the strains showed different mutant spectra and distinct evolutionary trajectories in mice (poliovirus mutates so rapidly that any infection is also an evolutionary process).
This study adds to a growing stack of evidence that the mutational neighborhood of the genetic sequences in a population profoundly shapes the potential to adapt. Many of these studies have been done in viruses such as the bacteriophage phi-6 (see Christina Burch and Lin Chao’s paper in Nature and Robert McBride, Brandon Ogbunugafor and Paul Turner’s paper in BMC Evolutionary Biology) with high mutation rates. It remains an open question how relevant mutational neighborhoods are for understanding adaptation in eukaryotes with more fidelitous replication and potentially smaller population sizes.
3. Cichlids Evolvability in the interaction between traits & ecology
I think that students are often a little baffled by the idea that patterns at different levels of evolution may need to be explained by distinct processes. Genomic changes may be largely neutral, while phenotypic changes might be generally adaptive; analogously, one set of factors might explain how well a taxon adapts, while another set might account for how often it speciates. Examples above show how evolvability can help bridge neutral and adaptive changes, but there’s also excited work looking at evolvability at the species level.
In a recent paper, published in Nature and available from the author’s website, Catherine Wagner, Luke Harmon, and Ole Seehausen try to explain which factors account for the astounding tendencies of African lake cichlids to radiate–rapidly form multiple species–within a single lake. What inspires me about this paper is that the authors look beyond this marvellous example of evolvability to ask a deep comparative question: why have so many lake cichlids failed to radiate? As the authors note, “…cichlids have independently diversified within African lakes on more than 30 occasions, and have colonized lakes without diversifying on more than 120 occasions.” The contrasting results of these many natural experiments provide the grist for a sophisticated statistical model which considers a range of possible explanation. The conclusion–that lake depth, solar energy input, and the strength of sexual selection all contribute to radiation potential–allow real predictions about what we’ll find in unstudied lakes, as well as in other examples of adaptive radiation.
1. E. coli. By Credit: Rocky Mountain Laboratories, NIAID, NIH [Public domain], via Wikimedia Commons