Chromosomes on shuffle: disentangling the relative contributions of natural selection, sexual selection, and drift on the evolution of a chromosomal inversion.

Project Information

ADAPTIVE INVERSIONS

Grant agreement ID: 704920

DOI

10.3030/704920

Project closed

EC signature date 22 February 2016

Start date 1 May 2016

End date 30 April 2018

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 173 857,20

EU contribution

€ 173 857,20

Coordinated by

GOETEBORGS UNIVERSITET
Sweden

Periodic Reporting for period 1 - ADAPTIVE INVERSIONS (Chromosomes on shuffle: disentangling the relative contributions of natural selection, sexual selection, and drift on the evolution of a chromosomal inversion.)

Reporting period: 2016-05-01 to 2018-04-30

Summary of the context and overall objectives of the project

Evolution is defined as a change in allele frequency over time. However, most work in the field of evolutionary biology concentrates on single nucleotide polymorphisms (SNPs) while other types of mutations (large insertions/deletions, structural rearrangements) are largely ignored. Chromosomal rearrangements, such as inversions (a piece of chromosome that is flipped relative to its normal orientation), are large-scale structural mutations that may encompass millions of nucleotides. Inversions segregate together as a single unit due to repressed recombination. Once thought to be relatively rare, the genomic revolution has revealed that inversions are orders of magnitude more common than previously thought and occur in a wide variety of taxa. Moreover, inversions are often found to have facilitated evolutionary processes such as adaptation and speciation. Despite their frequency and importance, we still lack an understanding of how and why inversions evolve. The key objective of this project was to strengthen our understanding of inversion evolution by systematically examining and disentangling the forces that govern the evolution of an inversion in a model species, the seaweed fly Coelopa frigida. Coelopa frigida inhabits “wrackbeds” (accumulations of decomposing seaweed) and has a paracentric inversion polymorphism on chromosome I (spanning 10% of the genome and containing at least 100 genes) that consists of an α and β version. Specifically, this research aimed to determine how natural and sexual selection govern the evolution of both regulatory and coding variation in an inversion polymorphism in C. frigida.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

During the project we have:
1. Conducted a large-scale whole genome re-sequencing study (60 genomes sequenced) to examine diversity and divergence within the inversion and to look for signatures of natural selection. This data revealed that α and β are highly divergent and that they contain more population specific variation than expected by chance. Re-analysis of this data using an updated genome assembly is currently ongoing. Together with colleagues we also developed a SNP marker for the inversion. This paper is published in Proceedings of the Royal Society B: https://doi.org/10.1098/rspb.2018.0519.

2. Examined a potential driver of adaptation, the microbiome of the wrackbed (the piles of rotting seaweed where C. frigida lives, and the sole food source for C. frigida larvae) in depth. We sequenced 16S DNA from both the wrackbed microbiome and the larval gut microbiome from 5 different populations across Scandinavia. This data revealed that wrackbed microbiomes are highly variable between populations but consistent within populations. The salinity of the surrounding water is a major factor driving this variation. Larval gut microbiomes were also highly variable but not related to the inversion genotype. This manuscript is currently in preparation.

3. Detailed the link between local environment, selection pressures on the inversion, and phenotypic effects of the inversion. We conducted a balanced reciprocal transplant experiment where C. frigida larvae were from 4 populations were raised on 4 substrates (seaweed) from all 4 populations. We examined changes in the frequencies of the karyotypes across populations and substrates as well as shifts in two phenotypes (body size and development time) known to be associated with the inversion. The results from this study indicated found that local environment strongly modified karyotype frequencies and that this effect differed between populations. Inversion-related phenotypes showed stable patterns but the magnitude of differences between groups was affected by population and substrate. The manuscript is currently in review and available on bioRxiv (https://doi.org/10.1101/295568).

4. Elucidated a signal for sexual selection in C. frigida (cuticular hydrocarbons) and investigated links between this signal, environmental conditions, and the inversion. Natural and sexual selection interact when traits are under both natural and sexual selection or when sexually selected traits are influenced by environmental conditions. We were interested in the signal used for sexual selection in C. frigida and if that signal could be linked to the inversion, the environment, or both. Cuticular hydrocarbons (CHCs) are often used as chemical signals in insects so we designed a study to: 1. Describe the CHC composition of C. frigida, 2. Determine the variance caused by population, diet, sex, and the inversion. We found significant effects of population, sex, diet, and the inversion. This suggests that CHCs are used as sexual signals in C. frigida and that they potentially represent a major intersection of natural and sexual selection. This manuscript is currently in review and can be found on bioRxiv (https://doi.org/10.1101/303206
).

5. Completed labwork for a gene expression study to determine the role of gene expression in inversion heterosis. The funding for RNA-sequencing has been secured and samples will be sequenced Summer/Fall 2018.


Results from this project have been presented at three international conferences with a third presentation scheduled for August 2018. One manuscript has been accepted, two are in review, and two are in preparation. We expect five other manuscripts to be generated from this work making a minimum total of nine. Significant engagement with the public has taken place via presentations of the project and C. frigida system to groups visiting Gothenburg University, the establishment of a photo contest bringing together scientists and the public, and media coverage of the project (two separate interviews with Swedish Radio).

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

This project has significantly advanced our knowledge of how inversions evolve in general and how they have evolved in C. frigida specifically. The research performed under this grant has been exceedingly interdisciplinary (combining population genetics, ecology, metagenomics, evolutionary genetics, chemical ecology, bioinformatics, and evolutionary theory) and generated a large amount of collaboration both within Gothenburg University (5 collaborators) and internationally (8 collaborators from 6 countries).

It is hoped that the ecological aspects of this work draw attention to the wrackbed environment as one of extreme importance and can be used to influence EU strategy for sustainable development. Coelopa frigida is one of few organisms that link marine and terrestrial habitats as their food source is marine bacteria that grow on macroalgae and they are prey items for shorebirds. Given the unique niche they occupy, they are potentially an important target for assessing ecosystem health.

Life stages of the seaweed fly and an example wrackbed (background)