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. Hablützel 1 , Alessia Cariani 3 , Jeroen Van Houdt 4 , Adriaan Rijnsdorp 5 , Fausto Tinti 3 , F ISH P OP T RACE 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

Content 1. Adaptation at high levels of gene flow 2. The seascape of a temperate flatfish 3. Take home message IFS10, Saint-Malo, 12.11.2017 2

1. Adaptation at high levels of gene flow For a long time it was thought to be highly unlikely that fish populations adapt under high levels of exchange. However, times change …. IFS10, Saint-Malo, 12.11.2017 3

Large population sizes should limit population differentiation … 1. It takes many thousands of generations to show any level of differentiation at large population sizes 2. Migration counteracts population differentiation at smaller population sizes Hauser and Carvalho, 2008 IFS10, Saint-Malo, 12.11.2017 4

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) IFS10, Saint-Malo, 12.11.2017 5

Adaptation under high levels of gene flow • 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) IFS10, Saint-Malo, 12.11.2017 6

Some typical traits of marine organisms • 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, …) IFS10, Saint-Malo, 12.11.2017 7

Conundrum … How to differentiate between gene flow and adaptation? = between neutral and adaptive processes? IFS10, Saint-Malo, 12.11.2017 8

Conundrum solved 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. IFS10, Saint-Malo, 12.11.2017 9

Seascape genomics • 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 IFS10, Saint-Malo, 12.11.2017 10

2. The seascape of a temperate flatfish It is now possible to identify not only neutral processes of evolution (drift and gene flow), but also adaptive processes in outbred non-model organisms. Adaptation is of course a well known genetic principle, especially in model organisms 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 : IFS10, Saint-Malo, 12.11.2017 11

Ecological context of sole Solea solea L. • 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 : o community structure and ecology o evolution • To what extent? IFS10, Saint-Malo, 12.11.2017 12

Economic characteristics of sole Important for the North Sea trawl fishery Sustainability is unfortunately low: rather destructive to the bottom fauna. IFS10, Saint-Malo, 12.11.2017 13

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) IFS10, Saint-Malo, 12.11.2017 14

Aims 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 15

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 Diopere et al. 2017 ICES J Mar Sci IFS10, Saint-Malo, 12.11.2017 16

Outlier loci • Outlier loci = SNPs with above average differentiation (F ST ) values • Might be due to historical reasons, hybridisation, adaptation, chance • Here: correlate outlier SNP with gene (regions) and phenotype & environment IFS10, Saint-Malo, 12.11.2017 17

3 or 4 groups? Biplots illustrate the similarities in allele frequencies of neutral & outlier loci and associations with environmental parameters Neutral SNPs Outlier SNPs 4 1 2 3 1 2’ 1 2 3 Diopere et al. 2017 ICES J Mar Sci IFS10, Saint-Malo, 12.11.2017 18

4 groups … Neutral SNPs Outlier SNPs IFS10, Saint-Malo, 12.11.2017 19

IBD of neutral & outlier SNPs, partitioned in 3 main groups. IBD of neutral & outlier SNPs, based on a regional approach. IBD is important IFS10, Saint-Malo, 12.11.2017 20

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

Function of outlier SNPs 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 . IFS10, Saint-Malo, 12.11.2017 22

Seascape genomics of sole Partitioning variance of environmental data and neutral & outlier SNPs with similarity fusion networks (SFN) - IBD - Local adaptation Diopere et al. 2017 ICES J Mar Sci Cold winters Inshore spawning Offshore spawning All loci Outlier loci Neutral loci

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? IFS10, Saint-Malo, 12.11.2017 24

Current management IFS10, Saint-Malo, 12.11.2017 25

Management conclusion 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 … IFS10, Saint-Malo, 12.11.2017 26

3. Take home message • 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 27

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 ! FishPopTrace was selected as an example of innovation and impact in Food Security in Horizon2020 Blue Growth Research and Innovation (17.11.2017) IFS10, Saint-Malo, 12.11.2017 28