Genes in parallel

Adaptation from genetic variation

One of the central themes of this blog, and indeed of evolutionary biology as a whole, is the notion that adaptation is often underpinned by genes. Genetic variation acts as the basis for natural selection to favour or disfavour traits: while this is directly through phenotypic traits (e.g. fur colour, morphology, behaviour), these traits are typically determined by a genetic component. In the early stages of adaptation, evolution can often be observed by changes in the frequency of genetic variants (alleles) within a species or population over time as natural selection acts, gradually leading to the observable (and sometimes dramatic) change in species over time.

GxPxE adaptation figure
How genotypes, phenotypes and the environment (i.e. the context of natural selection) are all linked. Phenotypic traits such as body colour are usually dictated by an underlying genotype (top row). In the natural world, variation in alleles at the genotype level creates variation in phenotypes within a given population (middle row). However, natural selection may preference some phenotypes over others: in this instance, blue fish are more cryptic and thus are less likely to be predated upon. This causes the associated alleles (the blue genes) to increase in frequency whilst the alternative allele (the orange genes) decrease in frequency. Note that natural selection acts on the phenotype first.

Genotype to phenotype

But as we’ve discussed before, this interaction between the underlying genotype and the phenotypic expression of an individual is not always straightforward. Single genes can have multiple resultant phenotypic traits (this effect is called ‘pleiotropy’), or different genes can interact with one another to form complex traits (such as through quantitative trait loci or in polygenic selection). Naturally, however, one might expect that any given gene has the same function in (at least semi-related) species, and that if that gene was under positive selection (i.e. favoured) in a particular environment then all species with that gene should show positive selection. After all, if it’s the same gene with the same function, why would it be different between species?

Is evolution predictable?

This is a key question within evolutionary biology and ecology, and one that is difficult to answer. While we might logically expect that the same genes that underlie the same phenotypic traits should be under natural selection in different organisms adapting to similar circumstances, this pathway is not clear nor universal. Even the same gene in different species might be associated with an entirely different physiological function and trying to connect genetic variation, phenotypic trait and adaptive ability (through measures of fitness) requires robust data and evidence that connects all three categories.

Pleiotropy vs polygenic figure
Some examples of the complex interaction between genotype and phenotype, which are discussed in more detail here. In pleiotropy (top example), a single gene might alter multiple different phenotypic traits, such as in albinism. Contrastingly, multiple different genes might together contribute to a single phenotypic trait if they demonstrate quantitative effects or act under polygenic selection.

In a large number of cases, studies may focus more strongly on one aspect (the genetic underpinning of adaptation; physiological traits evolving over time; or adaptive traits that are broadly most useful for dealing with a particular adaptive problem) and infer aspects of the other two. In the case of ecological genomics, particularly in non-model species, information on how identified adaptive genes relate to evolutionary changes is suggested based on the physiological function of genes (through molecular biological studies, usually) and likely relationship to the environment in question. Nevertheless, understanding how these three components relate to one another – and whether this relationship is consistent across related species independently adapting to a given environment – is a key question in evolutionary science.

So how do we approach this problem? Well, one key way is with empirical comparative studies of real-world adaptation. Often, those seeking to address parallel adaptation will use a study system that demonstrates multiple adaptations to a particular environment within a group of organisms: arguably the most renowned of these is with stickleback fish. These highly diverse fish occupy both freshwater and marine habitats, but curiously appear to have evolved specific adaptations to colonise freshwater (from a marine ancestor) more than once over history. This leads to the question at hand: each time a species has adapted to freshwater, and undergone the relevant evolutionary changes to allow it to persist, are the same genes utilised to generate the same traits?

sticklebacks figure
A demonstration of the parallel adaptation of sticklebacks, evolving from a marine ancestor (centre, red) to freshwater species (outer, blue) independently multiple times. Source: Bell & Foster, 1994 via the Friedrich Miescher Laboratory of Max-Planck-Gesellschaft

Now, you may remember the term convergent evolution and wonder how that factors in (or how it’s different to parallel evolution). In parallel evolution, similar species are adapting to the same environmental pressure – given their (relatively) similar evolutionary background, it seems possible that these could originate from the same genetic architecture. This contrasts with convergent evolution, which involves very different groups of organisms showing similar adaptations to a particular adaptive issue – think of flight in bats and birds. These two groups are highly different (occupying different Orders), but from a first glance one might make the assumption that they are not too different based on the presence of wings. However, scientific research has demonstrated how the two groups have used different evolutionary approaches to solving a common issue – flight.

Converget vs parallel evolution figure
An example of the difference between convergent and parallel evolution. In this example, we have multiple independent evolutionary transitions to a freshwater in fish (blue fish). However, many of these shared a relatively recent ancestor (red side), and would be considered parallel evolution (as they likely share recent ancestral genetic diversity). This contrasts with a highly divergent transition from orange to blue on the right: this might be considered convergent evolution when compared to the left side fish given their long history of isolation from one another (as indicated by the dashes in the tree).

Different methods can give the same answer

The evidence from empirical studies currently suggests that true evolutionary parallelism – adaptation to the same conditions from the same genetic variants – is relatively rare. Instead, it appears that there are many different genetic solutions (and varying degrees of parallelism) to the same evolutionary problem, and different species may utilise different genes in different ways to adapt to the same environmental stressor, even if the physiological outcomes of these differences are similar. The translation from genetic variation, to phenotype, to adaptive potential is a difficult pathway to determine and only gets more complicated as each transitional steps adds exponential layers of complexity and relevant parameters to the mix.

The difficulty in predictive or repeated evolution

These findings have a number of implications for evolutionary biology, conservation management and the diversity of life on the planet. Chiefly, however, they demonstrate just how hard it is to predict evolution as a process: naturally, factors beyond just having the right genetic variants and the right environmental stressor are important for adaptation. Understanding the nuance of when, or how, species adapt based on their own characteristics (such as total genetic diversity, life history traits or demographic history) may be key components to determining if or how species may evolve in the future. With the ongoing climate breakdown crisis, this becomes a key management issue as we strive to figure out which species are most threatened in the future and which ones might be able to evolve in response.

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