Periodic Reporting for period 4 - BARRIERS (The evolution of barriers to gene exchange)
Période du rapport: 2021-03-01 au 2022-02-28
Species are defined by their ability to interbreed and by their inability of breed successfully with other species. Thus, the formation of new species, a key step in the origin of biological diversity, is dependent on the evolution of traits that prevent interbreeding between populations that were previously part of one species. Closely-related species are typically isolated from one another by multiple traits of this type. However, the evolutionary origin of individual barrier traits and the ways in which multiple traits are brought together to form strong barriers are not well understood. At a time when biological diversity is under threat from rapidly changing environments and human-mediated dispersal, it is crucial to manage natural populations in ways that maintain evolutionary potential. This includes the potential to form new species. Therefore, understanding the speciation process is important both for interpreting and conserving biological diversity.
The focus of this project is on the accumulation of barriers to gene exchange and the processes underlying increasing reproductive isolation between populations that have gone part of the way to being new species. I use the power of natural contact zones, where these populations hybridize, combined with novel manipulative experiments and modern genetic techniques, to separate the processes that underlie differentiation between populations and the barrier effects of differentiated traits. The model system is a common coastal snail, Littorina saxatilis. In many places around Europe, this snail forms distinct populations adapted to different parts of the shore environment, with areas of hybridization where environments meet. Our objective is to understand the traits that reduce interbreeding and lower fitness of hybrids, the genetic basis of the traits and the way they combine to limit gene exchange. We then model the underlying processes to predict the circumstances in which populations are most likely to evolve complete reproductive isolation and so become new species.
Our project has advanced understanding of the speciation process. We have shown that it is nearer to completion in Spanish populations than in Swedish populations, probably because the contact there is older and more extensive. A particular form of genetic variant, chromosomal inversions, have been shown to be critical to the progress of adaptation and speciation through their effects of traits that fit organisms to their environment and also impact on mating behaviour.
The focus of this project is on the accumulation of barriers to gene exchange and the processes underlying increasing reproductive isolation between populations that have gone part of the way to being new species. I use the power of natural contact zones, where these populations hybridize, combined with novel manipulative experiments and modern genetic techniques, to separate the processes that underlie differentiation between populations and the barrier effects of differentiated traits. The model system is a common coastal snail, Littorina saxatilis. In many places around Europe, this snail forms distinct populations adapted to different parts of the shore environment, with areas of hybridization where environments meet. Our objective is to understand the traits that reduce interbreeding and lower fitness of hybrids, the genetic basis of the traits and the way they combine to limit gene exchange. We then model the underlying processes to predict the circumstances in which populations are most likely to evolve complete reproductive isolation and so become new species.
Our project has advanced understanding of the speciation process. We have shown that it is nearer to completion in Spanish populations than in Swedish populations, probably because the contact there is older and more extensive. A particular form of genetic variant, chromosomal inversions, have been shown to be critical to the progress of adaptation and speciation through their effects of traits that fit organisms to their environment and also impact on mating behaviour.
We have characterized the genome-wide pattern of genetic differentiation across one contact zone in Sweden. This has revealed unexpected patterns indicating that chromosomal rearrangements may be important in the divergence process. Subsequently, we have collected new samples, with extensive documentation of phenotypes, from additional Swedish sites and for sites in Spain, for different seasons and cohorts. In Sweden, we see strong replication of patterns, reinforcing the evidence for the role of chromosomal rearrangements in local adaptation. A crossing study has also shown that these rearrangements contribute to the genetic determination of key adaptive traits. In Spain, we see a much stronger barrier to gene flow but one that is still associated with the same chromosomal rearrangements. We are working to understand the reasons for the stronger barrier. The wide-spread rearrangements contribute to local adaptation on at least two environmental axes and they are likely to be old. Simulation work has shown how old inversions can be maintained by the accumulation of deleterious recessive mutations. We have published a perspective article contributing to the current debate about the evolutionary significance of chromosomal rearrangements.
We have also studied mate choice, both directly by observing mating behaviour and indirectly through collecting offspring for genotyping. Combined with modelling results, this has provided novel insights into the way sexual selection can enhance barriers to gene flow, even when it operates in the same direction in both diverging populations. We have conducted a series of experiments aimed at understanding habitat choice. We have also analysed embryo abortion, a possible form of incompatibility that might also contribute to reducing gene exchange. Modelling of the system is continuing, now focusing on the role of chromosomal rearrangements.
These results have been published in 20 scientific articles to date and an animated video explaining our results to a wider audience is freely available to the public and for educational purposes (https://www.youtube.com/watch?v=XDAuQQzQuWg&t=1s).
We have also studied mate choice, both directly by observing mating behaviour and indirectly through collecting offspring for genotyping. Combined with modelling results, this has provided novel insights into the way sexual selection can enhance barriers to gene flow, even when it operates in the same direction in both diverging populations. We have conducted a series of experiments aimed at understanding habitat choice. We have also analysed embryo abortion, a possible form of incompatibility that might also contribute to reducing gene exchange. Modelling of the system is continuing, now focusing on the role of chromosomal rearrangements.
These results have been published in 20 scientific articles to date and an animated video explaining our results to a wider audience is freely available to the public and for educational purposes (https://www.youtube.com/watch?v=XDAuQQzQuWg&t=1s).
Our first contact zone study introduced new methods for detecting parts of the genome that are influenced by divergent natural selection. Together with our genome assembly and genetic map, this revealed a surprising concentration of selection in specific genomic regions. We have since provided evidence that these patterns result from the presence of multiple chromosomal inversions that contribute to divergence between populations but remain polymorphic within populations. This changes our view of how genome rearrangements can contribute to adaptation and speciation and we have discussed this changing view in a perspective article as well as collaborating to model aspects of inversion evolution. Our methods for the analysis of the contribution of chromosomal inversions to genetic variation in key traits advance the tools available in this field and our replicated contact zone study sets new standards for sampling and analysis.
Our work on assortative mating and sexual selection adds a new dimension to the role of sexual selection in speciation and introduced novel approaches to documenting mating patterns and assessing their impact on gene exchange.
We are also finding surprising evidence for very strong barriers to gene flow in the Spanish populations but need further work to understand this properly.
We have generated a new method for deriving shell growth parameters from two-dimensional images that will be useful to many other groups as well as giving us new insight into the basis of shape divergence in our system.
We have discovered a surprising association between local adaptation, sex-specific divergence and sex determination in Swedish snails. This promises to provide new insight into sexually-antagonistic selection during divergence and speciation.
Our work on assortative mating and sexual selection adds a new dimension to the role of sexual selection in speciation and introduced novel approaches to documenting mating patterns and assessing their impact on gene exchange.
We are also finding surprising evidence for very strong barriers to gene flow in the Spanish populations but need further work to understand this properly.
We have generated a new method for deriving shell growth parameters from two-dimensional images that will be useful to many other groups as well as giving us new insight into the basis of shape divergence in our system.
We have discovered a surprising association between local adaptation, sex-specific divergence and sex determination in Swedish snails. This promises to provide new insight into sexually-antagonistic selection during divergence and speciation.