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flatfish reveals selection under high levels of gene flow Filip - - PowerPoint PPT Presentation

Seascape genetics of a flatfish reveals selection under high levels of gene flow Filip A.M. Volckaert 1 , Eveline Diopere 1 , Sara G. Vandamme 1, 2 , Pascal I. Habltzel 1 , Alessia Cariani 3 , Jeroen Van Houdt 4 , Adriaan Rijnsdorp 5 , Fausto


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Seascape genetics of a flatfish reveals selection under high levels of gene flow

Filip A.M. Volckaert 1, Eveline Diopere 1, Sara G. Vandamme 1,

2, Pascal I. Hablützel 1, Alessia Cariani 3, Jeroen Van Houdt 4,

Adriaan Rijnsdorp 5, Fausto Tinti 3, FISHPOPTRACE Consortium, Gregory E. Maes 1,4

1 Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, B 2 ILVO-Fisheries, B-8400 Oostende, B 3 Department of Biological, Geological and Environmental Sciences, University of

Bologna, I-40126 Bologna, I

4 Center for Human Genetics, Genomics Core, ON 1, University of Leuven and

UZ Leuven, B-3000 Leuven, B

5 Wageningen Marine Research, NL-1970 AB IJmuiden, NL

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Content

  • 1. Adaptation at high levels of gene flow
  • 2. The seascape of a temperate flatfish
  • 3. Take home message

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  • 1. Adaptation at high levels of gene flow

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For a long time it was thought to be highly unlikely that fish populations adapt under high levels of exchange. However, times change ….

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Large population sizes should limit population differentiation …

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Hauser and Carvalho, 2008

  • 1. It takes many thousands
  • f generations to show any

level of differentiation at large population sizes

  • 2. Migration counteracts

population differentiation at smaller population sizes

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Adaptation at large population sizes

However, even in very large populations with low levels of drift, local adaptation exists (Hauser and Carvalho, 2008) Adaptation is observed at the fitness level, for example

  • spring and fall spawning Atlantic herring (Gaggiotti et al. 2009)
  • coastal and migratory Atlantic cod (Berg et al. 2016)
  • Iron adapted picocyanobacteria (Prochlorococcus) (Farrant et al. 2016)

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Adaptation under high levels of gene flow

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  • What if and high gene flow levels and adaptation cooccur?
  • It’s called isolation with migration (Sousa and Hey, 2013); there is migration

between population, each with its distinct fitness profile.

  • Fitness difference may relate to a single gene mutation (e.g. body

color) or multiple low impact mutations (polygenic)

  • In a polygenic situation many islands of selection (= soft selection

sweep) characterize the genome (Bernatchez, 2016)

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Some typical traits of marine organisms

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  • Large population sizes
  • High potential for gene flow (larva and/or adult)
  • Large number of progeny
  • Low survival rate  high selection pressure
  • Adapted to local conditions
  • Also: increasingly adapted to global change (pollution,

temperature, pH, …)

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Conundrum …

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How to differentiate between gene flow and adaptation? = between neutral and adaptive processes?

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Conundrum solved

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Neutral processes impact the full genome because they are the consequence of population dynamics Adaptive processes affect sections (islands) of the genome because they impact selected genes and gene regions. High-throughput genomics (big data!) facilitates the large-scale scan of the genome to recognize neutral and adaptive regions.

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Seascape genomics

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  • But we aim higher….
  • What are the causes of the adaptive landscape?
  • Solution: high-throughput genomics (big data) + population

genetics + environmental data (big data) + location = SEASCAPE

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  • 2. The seascape of a temperate flatfish

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It is now possible to identify not only neutral processes of evolution (drift and gene flow), but also adaptive processes in outbred non-model

  • rganisms.

Adaptation is of course a well known genetic principle, especially in model

  • rganisms such as Arabidopsis, Drosophila and mouse, crops and farm animals (as a

result of directional selection), and man (lactose tolerance).

If outbred organisms are an option, than commercial fish populations are first in line. Here we focus on the drivers of population differentiation in a common flatfish of the European coastal seas :

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Ecological context of sole Solea solea L.

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  • Flatfish dominate the soft bottom community of the North

Sea

  • Sole is a common member (after plaice)
  • Highly dynamic environment (tidal & wind mixing)
  • Hence high primary productivity
  • Considerable human interference on :
  • community structure and ecology
  • evolution
  • To what extent?

IFS10, Saint-Malo, 12.11.2017

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Economic characteristics of sole

Important for the North Sea trawl fishery Sustainability is unfortunately low: rather destructive to the bottom fauna.

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Connectivity of sole

  • Dispersal of juveniles at scale of ˜10 km (Le Pape and Cognez

2016) and adults at ˜150 km (Burt and Millner 2008); modeling at

˜100 km (Lacroix et al. 2017).

  • Isolation by distance :

Kotoulas et al (1995) 100 km; Cuveliers et al. (2011)

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Aims

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Differentiate between the neutral and adaptive genetic structure in the natural environment Point to the cause(s) of local adaptation

IFS10, Saint-Malo, 12.11.2017

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Approach

  • Range-wide sampling
  • 17 samples; n = 539
  • Genotyping with 426 SNPs

sourced from muscle transcriptome

  • 19 outlier loci (Lositan &

Bayescan)

  • Environmental data: SST,

salinity, mixed layer depth, chlorophyll

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Diopere et al. 2017 ICES J Mar Sci

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Outlier loci

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  • Outlier loci = SNPs with above average differentiation (FST)

values

  • Might be due to historical reasons, hybridisation,

adaptation, chance

  • Here: correlate outlier SNP with gene (regions) and

phenotype & environment

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3 or 4 groups?

Biplots illustrate the similarities in allele frequencies of neutral & outlier loci and associations with environmental parameters

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1 2 2’ 3 1 2 1 3 4

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Diopere et al. 2017 ICES J Mar Sci

Neutral SNPs Outlier SNPs

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4 groups …

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Neutral SNPs Outlier SNPs

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IBD of neutral &

  • utlier SNPs,

partitioned in 3 main groups. IBD of neutral &

  • utlier SNPs, based
  • n a regional

approach.

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IBD is important

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Seascape genomics of sole

Associate genetic variation with environmental and spatial variability through Redundancy analysis (RDA) Important factors:

  • Neutral SNPs: space + environment explain 65% of the neutral

variation and are highly intertwined

  • Outlier SNPs: no significant contribution
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Function of outlier SNPs

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So what is the functional importance of these outlier SNPs? 15 out of 19 SNPs have been annotated (= assigned a putative function)

  • troponin T fast skeletal muscle isoform: growth and contraction of skeletal muscle
  • cytoskeletal protein cytokeratin 13: expressed in internal stratified and mucus secreting

epithelia of fish

 growth related (not unexpectedly!) But there are much more genes involved in adaptation! Next step: high resolution genome mapping based on transcriptome

(Benzekri et al., 2014), linkage mapping (Diopere et al. 2014) and full genome

sequencing.

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Seascape genomics of sole

Partitioning variance of environmental data and neutral &

  • utlier SNPs with similarity fusion networks (SFN)
  • IBD
  • Local adaptation

Neutral loci All loci Outlier loci

Diopere et al. 2017 ICES J Mar Sci Cold winters Inshore spawning Offshore spawning

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Conclusions

Sole populations of the Northeast Atlantic Ocean show:

  • Isolation by distance
  • Local adaptation : matches with behaviour (in/offshore spawning differentiates

North Sea/English Channel from Bay of Biscay) and environment (winter mortality linked to Sea Surface Temperature in North Sea)

 Matches with ecological (Amara et al. 2000) and phenotypic evidence

(Rijnsdorp et al. 1992)

How may this translate to fisheries management?

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Current management

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Management conclusion

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It is possible to simplify management as the currently implemented stock structure is of a finer resolution than natural population units show. Will this be implemented? Unlikely …

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  • 3. Take home message

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  • Sole has a high level of connectivity
  • Adaptation is linked to environment and behaviour
  • Spatial organisation of fisheries management seems fine
  • But other factors shouldn’t be neglected: population size

and structure (don’t forget the old folks), and sex ratio.

IFS10, Saint-Malo, 12.11.2017

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Acknowledgements

LBEG team : Els Cuveliers, Bart Hellemans and Federico Calbolli ILVO – Fisheries: Johan Robbens Wageningen Marine Research Numerous colleagues providing samples EU project FishPopTrace: Gary Carvalho and colleagues

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! FishPopTrace was selected as an example of

innovation and impact in Food Security in Horizon2020 Blue Growth Research and Innovation (17.11.2017)