Mapping migration and adaptation in genomes

Project Information

MAPGenome

Grant agreement ID: 799729

DOI

10.3030/799729

Project terminated on 30 November 2019

EC signature date 27 February 2018

Start date 1 March 2018

End date 29 February 2020

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 148 635,60

EU contribution

€ 148 635,60

Coordinated by

FCIENCIAS.ID - ASSOCIACAO PARA A INVESTIGACAO E DESENVOLVIMENTO DE CIENCIAS
Portugal

Periodic Reporting for period 1 - MAPGenome (Mapping migration and adaptation in genomes)

Reporting period: 2018-03-01 to 2020-02-29

Summary of the context and overall objectives of the project

Understanding the interplay of adaptation and migration at the genomic level is a fundamental goal of evolutionary biology, with wide applications in situations where these two forces operate, e.g. pesticide resistance or species invasion. These processes underlie emergent societal concerns, reflected in EU policies priorities, in agriculture, global change biology, and human health. Yet, this goal remains largely elusive, mainly because genetic signatures of local adaptation are confounded by other evolutionary processes, such as past demography, the removal of deleterious mutations and recombination rate variation. We moved towards achieving this goal by combining theoretical results and development of bioinformatics methods, with experimental evolution and genome-wide data from both experimental and natural populations. We focused on a major crop pest, the spider mite Tetranychus urticae, with a haplo-diploid mode of reproduction. Our modeling results predict that divergent selection is more efficient in haplo-diploids than diploids in scenarios with gene flow. As a result, such species can diverge even with migration. To test these predictions, we are using experimental evolution, following spider mite populations adapting to a new environment under controlled conditions, with and without migration. We are quantifying changes through time in life-history traits and genomic patterns. Preliminary results indicate a slower rate of adaptation in treatments with migration. Moreover, we are finishing the development of a bioinformatics method to map variation in gene flow across the genome, which can be used by other researchers. Finally, to study the impact of gene flow we analyzed genomic data from natural populations from different systems (fish to primates). Results support that genetic signatures of past gene flow are widespread across systems. In sum, we contributed to move the field towards a comprehensive characterization of the genomics of adaptation in face of gene flow. The theory, methods and data resulting from this MSCA will be of general application to address fundamental questions on speciation and ecology, while providing a transferable framework to tackle societal challenges, from agriculture to global change.

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

The work performed so far includes:
a) New theoretical results on the interplay of gene flow and selection. Since T. urticae is a haplo-diploid species, we derived analytical results and used SLIM v3.3 simulations for species with such mode of reproduction. Our results indicate that divergent selection is more efficient in haplo-diploids than diploids in models with gene flow. Also, we show that deleterious mutations (i.e. mutations with a negative impact in fitness) can lead to heterogeneous genomic patterns. Depending on the recombination rates, selective and dominance coefficients we predict a transition from associative over-dominance (AOD) to background selection (BGS). As a result of the secondment, together with Prof. Daniel Wegmann we worked on a bioinformatics method to infer variation of migration along the genome, which we expect to release during 2020 (publicly available on GitHub). These results were disseminated at conferences (e.g. ENBE, SMBE) and two manuscripts are in preparation.

b) To test theoretical predictions from a), we are performing experimental evolution, exposing mites to tomato host-plants in different environments with and without migration. We used simulations to provide experimental guidelines for studying adaptation with experimental evolution (published in Sousa et al. 2019 COIS). Since many host-plant species (e.g. tomato) accumulate heavy metals (e.g. Cadmium) as a defense against herbivores (e.g. T. urticae), we treat Cadmium presence as a challenging environment. We have three treatments: (i) no Cadmium (environment A) without migration; (ii) Cadmium (environment B) without migration; (iii) Cadmium (environment B) receiving migrants from environment A every generation. We optimized protocols for DNA extraction for pools of spider mites. We are measuring changes in relevant life-history traits (e.g. fertility, mortality, etc.) and genomic patterns through time. Preliminary results indicate that migration slows the rate of adaptation. We plan to submit a manuscript by the end of 2020.

c) To investigate these processes in natural populations, we have analyzed genome-wide population data from three systems: (i) recent divergence in stickleback fish; (ii) old divergence of Iberian freshwater fish of genus Squalius; (iii) divergence of bonobos and chimpanzees. Results were published in peer-reviewed journals, supporting that genetic signatures of past gene flow are widespread across different systems, pointing to its evolutionary relevance.

Finally, I was involved in activities to disseminate this MSCA results to a wider audience. For instance, I participated in FCUL Open Day 2019, Speed Dating with Scientists 2019, gave seminars for a general audience of students and researchers (e.g. Celebration of Statistics Day, Ecological Modeling Day), I gave two interviews for a generalist radio ( “Ponto de Partida” and “Dias do Futuro” – Antena 1).

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)

We have investigated how populations adapt in face of gene flow, taking an integrative approach combining my expertise in genomics with the expertise in experimental evolution of the project supervisor Prof. Sara Magalhães, resulting in a successful two-way exchange of knowledge.

Our theoretical results indicate that divergent selection is more efficient in haplo-diploid than diploid species, leading to different genomic differentiation patterns in haplo-diploid species, generating predictions that can be tested. This suggests that haplo-diploids, such as the crop pest T. urticae, adapt faster and tolerate more migration than diploid species. This has important implications as it can be related to the ability of T. urticae to use a wide-range of host-plants and evolve rapidly pesticide resistance.

Moreover, our simulation results suggest that background selection (BGS) is prevalent in haplo-diploids. Surprisingly, for slightly deleterious recessive mutations we predict genomic patterns consistent with associative overdominance (AOD), seen for diploids irrespective of migration. Importantly, we found that genomic regions of high recombination are not affected by AOD nor BGS and hence such regions can be used as a benchmark. This opens new lines of research, guiding developments to detect genes affected by deleterious mutations, which can have wide impacts, ranging from conservation to human genetics.

By combining my knowledge in genomics, with the supervisor’s knowledge in experimental evolution, we designed an experiment to quantify the impact of migration on adaptation. We quantified changes in life-history traits and in genomic patterns, comparing scenarios with and without gene flow. These results will be novel, as little is known about gene flow from studies in controlled environments.

In this project we applied genomic tools to address how crop pests adapt to novel environments. Results can help us predict how crop pests respond in scenarios with increasing levels dispersal and migration due to global change, including invasion of new geographic areas and new host plants. Characterizing the genomic and evolutionary processes involved in how populations adapt in face of gene flow is thus of utmost applied and fundamental importance.

MAPGenome MSCA summary