Parallel evolution happens when similar phenotypes evolve repeatedly in multiple geographical locations, in response to similar selection pressures.
Littorina saxatilis is a very good system to study parallel evolution, as similar ecotype pairs have evolved repeatedly across Europe, eg in Sweden, Spain and the UK: Small snails on cliffs, adapted to wave exposure ("Wave ecotype"), and large snails on boulder fields, adapted to crab predation ("Crab ecotype").
However, the fact that similar phenotypic divergence is observed across locations does not tell us much about the similarity of the genetic basis. Do the same loci underlie divergence in different geographical locations? We use a combination of extensive sampling and genomic data analyses to answer this question.
Our work has shown that the similarity of the genetic basis increases with geographical proximity, potentially explained by higher levels of gene flow or a more recent shared history when locations are close. We have also shown that several chromosomal inversions are associated with divergence in all studied locations.
The evolution of strong reproductive isolation
One of the major goals of speciation research is to understand the forces and factors that influence the strength of reproductive isolation (RI) between populations.
The genus Littorina is an excellent system for studying this problem, because RI is highly variable between populations. For example, barriers to gene flow between the crab and wave ecotypes of Littorina saxatilis are relatively weak. In contrast, RI between L. saxatilis and its close relative L. arcana, is very strong and appears to have a genome-wide impact.
One goal of our research is to use genome sequencing and lab experiments to understand the basis and drivers of RI between L. arcana and L. saxatilis.
The most obvious candidate for a barrier trait is the difference in female reproductive strategy between the taxa, which includes a difference in both the mode (egg-laying in L. arcana vs. brooding in L. saxatilis) and timing of reproduction. However, other barriers, including assortative mating and microhabitat choice, may also play important roles.
By contrasting these results with studies of other littorinids, we hope to advance our understanding of the factors that advance speciation both in the genus and more generally.
Using hybrid zones to understand local adaptation and speciation
Hybrid zones are narrow regions in which genetically distinct populations meet, mate and produce hybrids. The balance between selection and gene flow in hybrid zones results in clines in both phenotypes and allele frequencies that can be very informative about both the nature of selection and the genetic basis of selected traits.
In Littorina, we see repeated contact zones at boundaries between habitats. We are using analysis of clines in phenotypes and genome-wide genetic markers to understand which regions of the genome experience barriers to gene flow, which traits are under selection and which environmental variables are the primary drivers of divergence.
Our results so far demonstrate that there is a genome-wide barrier to gene flow in Swedish contact zones between the Crab and Wave ecotypes.
Divergence patterns are strongly shared among replicate zones. However, the genomic architecture of divergence is dominated by chromosomal inversions.
Clines tend to be displaced from the main habitat boundary in a consistent direction but we do not yet understand why this is. We are now comparing these Swedish contact zones with zones in Spain where barriers are expected to be stronger.
Assortative mating and habitat choice
Two adjacent populations can live in distinct habitats and evolve divergent trait values. This can also affect mate choice and habitat choice.
For example, one or more divergent traits can mediate mating in such a way that its probability is reduced between the two divergent populations and/or can influence dispersal in a way that each population prefers its own habitat.
The first situation is known as assortative mating and the second one is referred to as habitat choice. What these two mechanisms have in common is a reduction of gene flow between the two ecologically divergent populations and the potential to contribute to the formation of new species.
Estimating the contribution of habitat choice and mate choice to reproductive isolation is one of the main research aspects of the Littorina team.
In L. saxatilis, the barrier strength of assortative mating is estimated using computer simulations based on the mating pattern observed across two different habitats, a crab-rich and wave-exposed habitat connected by a hybrid zone. The barrier strength of habitat choice is assessed by recording individual movements of tagged snails that were firstly sampled from either one of the two habitats or the hybrid zone and then released to either one of the two habitats or the hybrid zone.
Despite the discovery of a large number of loci implicated in adaptive divergence and reproductive isolation between ecotypes, until a couple of years ago, their position in the genome was unknown.
However, joint efforts to develop genomic resources for this system, including the assembly of a reference genome, linkage maps and population genomic data from a Swedish hybrid zone enabled the first characterisation of the genomic architecture of divergence between L. saxatilis ecotypes in 2018. This revealed 17 polymorphic inversions many of which are enriched for loci involved in adaptation of ecotypes to different environmental axes. The same inversions play a role in multiple localities, suggesting an important role in parallel evolution.
Recent findings further suggest that some inversions may even be present in closely related species, supporting a relatively ancient origin.
Ongoing work on this topic involves
characterising the inversion breakpoints at a higher resolution, including improving the genetic map and the reference genome assembly
inferring the evolutionary history of inversions
understanding the evolutionary processes involved in their origin, maintenance and evolution