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Chromosomal rearrangements and diversification on environmental gradients

Periodic Reporting for period 1 - INVERTIDAL (Chromosomal rearrangements and diversification on environmental gradients)

Reporting period: 2016-09-01 to 2018-08-31

Rocky shores usually comprise a heterogeneous environment with steep gradients of several physical factors and biological interactions, providing a natural laboratory to study local adaptation and ecological speciation. The marine gastropods of the genus Littorina, in particular L. saxatilis, have been increasingly recognised as one of the most interesting model systems to study these processes in the intertidal zone. Multiple ecotype pairs (‘Crab’ and ‘Wave’) of this species have independently diverged across the intertidal gradient of different geographic regions (Sweden, UK and Spain), as a response to similar selective pressures (crab predation and wave exposure, respectively). Despite the evidence in favour of parallel phenotypic divergence and reproductive isolation between L. saxatilis ecotypes, until the beginning of this project the main genomic regions influenced by natural selection and their distribution across the genome were largely unknown. Moreover, although the importance of chromosomal rearrangements (e.g. inversions) in adaptation and speciation is widely recognised, knowledge about their role in diversification was still limited to some taxa and had not yet been thoroughly investigated in molluscs. Benefiting from genomic resources that became available for L. saxatilis (e.g. reference genome and linkage map), INVERTIDAL tried to fill this gap by assessing the impact of inversions on the origin of phenotypic diversity observed in L. saxatilis.

Leveraging on the potential of the L. saxatilis system and of emerging genomic tools, four main goals were defined: i) test for the presence of chromosomal rearrangements, inversions in particular, in this system; ii) evaluate the role of inversions in local adaptation, ecotype evolution and reproductive isolation between L. saxatilis ecotypes; iii) quantify the level of sharedness of inversions involved in adaptation and diversification among countries; and iv) assess the main processes contributing for a sharedness of inversions (standing genetic variation in the ancestral population that expanded versus gene flow).
In order to achieve these goals, seven main tasks were implemented at the Department of Animal and Plant Sciences (University of Sheffield) under the supervision of Prof. Roger Butlin and with the collaboration of Prof. Marian Rocchi (University of Bari, Italy), Prof. Juan Pasantes (University of Vigo, Spain) and Prof. Tomas Marques-Bomet (University Popmpeu Fabra, Spain): i) detection of chromosomal rearrangements (in particular, inversions) using comparative and population genomics approaches; ii) validation of candidate inversions using recombination information obtained from sequencing four lab-reared families and cytogenetics tools; iii) characterisation of the genetic diversity associated with each inversion genotype; iv) cline analysis of the candidate inversions across a hybrid zone to infer signatures of selection; v) assessment of the relevance of inversions for genome-wide patterns of differentiation between two ecotypes across multiple sites (from Sweden to Spain); vi) quantification of the level of sharedness of outlier loci between populations, and the contribution of inversions to a shared genetic basis of parallel ecotype evolution; and vii) development of an Approximate Bayesian Computation approach to infer the evolutionary history of inversions and ecotypes.

Results overview
The data obtained during the project resulted in the following main findings: i) seventeen candidate inversions were detected across a hybrid zone between ecotypes in Sweden (Figure 1), most of which supported by recombination patterns from lab-reared families; ii) eleven out of the 17 inversions present a clinal distribution across the hybrid zone transect, suggesting the influence divergence selection; iii) most of the arrangements do not reach fixation in one of the transect ends, suggesting that balancing selection is also shaping the frequencies of these inversions in the system; iv) differentiation between ecotypes tends to be higher within the inverted regions. However, differentiation within some inversions is geographically localized, suggesting different frequencies or a different genetic composition oi inversions among locations; and v) inversions contribute to increase the percentage of shared outliers among locations, which tends to be higher between geographically close populations.
The results of INVERTIDAL will contribute to make the L. saxatilis system as one of the best models to study the role of chromosomal rearrangements in adaptation and speciation with gene flow, contributing to downgrade the Drosophila-centric knowledge about these processes. The number of rearrangements detected, as well as the evolutionary forces involved in their maintenance (divergent and balancing selection), open news avenues of research with general relevance for the field of evolutionary biology. By contributing to improve our understanding of the genetic basis of adaptation, and in particular, on the role of inversions in facilitating adaptation across environmental gradients, this project provided key information that will enable to improve our predictions about the species response to climate change, one of the main societal challenges of our time. Finally, the skills I developed with INVERTIDAL and the manuscripts already published (as well as those that will be soon submitted), put me in a very competitive position to establish as an independent scientist and start my own research group.