Evaluating the adaptive potential of the European eel: is the immunogenetic status recovering?

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Introduction

Material and Methods

Study scheme

Neutrally evolving mitochondrial marker

Genetic estimates of diversity, population differentiation and demography

Neutrally evolving nuclear markers

Genetic estimates of diversity, differentiation and demography amongst freshwater locations

Genetic estimates of diversity, differentiation and demography— inter-generation level

Adaptive marker: diversity and demography of the MHC

Results

Neutrally evolving mitochondrial DNA

Molecular indices, population structure and demography amongst sampling locations

Molecular indices, population structure and demography between generations

Neutrally evolving nuclear markers

Molecular indices, population structure and demography amongst locations

Molecular indices, structure and demography between generations

Adaptive marker: the MHC

Molecular indices and population structure

Screening for novel genetic diversity through events of gene conversion

Testing for positive selection

Demography and historical profile of MHC genetic diversity

All mismatch distributions indicated a clear deviation from a constant population size, fitting a scenario where a major demographic event occurred (Figs. 4 and 5). The frequency distribution of pairwise differences showed different peaks for both PSS (Fig. 4) and nPSS (PSS pairwisedifferences = 20; nPSS pairwisedifferences = 10) (Fig. 5). Those peaks reflect old lineages that are maintained in genes exhibiting trans-species polymorphism as is expected of the MHC (Klein, Sato & Nikolaidis, 2007) and recently reported for the European eel (Bracamonte, Baltazar-Soares & Eizaguirre, 2015). It was also possible to observe peaks in PSS and nPSS in the frequency of pairwise differences equaling 1. Those peaks are suggestive of increases in genetic diversity. No differences in the demographic profiles were detected between “silver eels” and “glass eels” (Figs. 4 and 5).

Discussion

Location-specific patterns of genetic diversity and demographic estimates

Genetic diversity and demographic estimates between age cohorts

Recruitment decline of the 1980s did not affected genetic estimates of neutral evolving markers

MHC reveals signatures of selection

Contemporary loss of MHC diversity: evidence of selection?

Limits of the study

Conclusions

Supplemental Information

mtDNA Haplotypes sequences and frequencies

DOI: 10.7717/peerj.1868/supp-1

Microsatellite allelic frequencies

DOI: 10.7717/peerj.1868/supp-2

MHC allelic frequencies

DOI: 10.7717/peerj.1868/supp-3

Pairwise distance matrix (FST) amongst sample locations

Pairwise distance matrix amongst sample locations. Above the diagonal are the values obtained with microsatellites, below the diagonal the ones obtained with mtDNA. Significant pairwise comparisons (p < 0.05) are depicted with *, or ** after correction for multiple comparison after (Narum, 2006).

DOI: 10.7717/peerj.1868/supp-5

Estimates of effective population size (Ne)

Estimates of effective population size (Ne) for each of the replicates, with respective confidence intervals.

DOI: 10.7717/peerj.1868/supp-6

Molecular indices of MHC for the sampled locations

- nHap, number of haplotypes; S, segregation sites; Hd, Haplotype diversity; π, nucleotide diversity; k, average number of differences; nr alleles/ind, average number alleles per individual with respective standard error (se); distnt, average nucleotide distance per individual with respective standard error (se).

DOI: 10.7717/peerj.1868/supp-7

Summary of codon-based tests for selection

ω = (dNdS), the ratio of non-synonymous (dN) per synonymous (dS) substitutions; LRT, likelihood ratio statistic for β + = α (null or no selection) vs β + unrestricted (alternative or episodic selection).

DOI: 10.7717/peerj.1868/supp-8

Sampling locations of individuals screened with neutral markers

Sampling sites and respective number of individuals (n) collected for each site and used for mtDNA and microsatellite analyses. Blue dots represent locations where “silver eels” where collected, yellow dots represent locations where “glass eels” where collected and the red dot represents location where both were collected. The G_p prefix stands for “glass eels”. Three numbers for the location of G_AD (Adour) depicts the n for three sampling events: G_AD2010, G_AD2011 and G_AD2012 respectively. The remaining acronyms have the following meaning: LC (Larne Lagoon), BT (Bann Toome), Q (Quoile), BU (Burrishole), BL (BannLower), SLC (LoughComber), DK (Denmark), LL (LarneLagoon), SLB (Boretree), GL (Glynn Lagoon), FI (Finland), PT (Portugal), Ger (Germany), G_BU (Burrishole), G_BNIRL (Northern Ireland), G_VSWE (Sweden), G_TENG (England), G_EGER (Germany), G_OSPA (Spain), G_VFRA (France), G_WENG (England), G_TITA (Italy), G_NIRL (Northern Ireland).

DOI: 10.7717/peerj.1868/supp-9

Sampling locations of individuals screened for the MHC

Labels are the same as in the previous picture.

DOI: 10.7717/peerj.1868/supp-10

STRUCTURE plot run with k = 26, where 26 are the number of sampled locations

DOI: 10.7717/peerj.1868/supp-11

Average distribution of allele frequencies for “silver” and “glass eels”

Above is shown the average distributions of allele’s frequency classes for “silver eels” (grey bars) and “glass eels” (open bars). Error bars represents the maximum and minimum number of alleles observed amongst replicates. Values on the Y-axis were obtained by multiplying the number of alleles, (k), with the frequency of the respective class. For purposes of visualization, all values were transformed to their square roots.

DOI: 10.7717/peerj.1868/supp-12

Density distributions of the three replicate Markov chain runs

Both the skyline (A), posterior (B) and likelihood (C) overlap, conferring statistical support for the shape of the Bayesian plots produced with MHC data (Figs. 4 and 5 of the main text).

DOI: 10.7717/peerj.1868/supp-13

Additional Information and Declarations

Competing Interests

The authors declare there are no competing interests.

Author Contributions

Miguel Baltazar-Soares conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables.

Seraina E. Bracamonte performed the experiments, contributed reagents/materials/ analysis tools, reviewed drafts of the paper.

Till Bayer and Frédéric J.J. Chain analyzed the data, contributed reagents/materials/ analysis tools, reviewed drafts of the paper.

Reinhold Hanel and Chris Harrod contributed reagents/materials/analysis tools, reviewed drafts of the paper.

Christophe Eizaguirre conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper.

Animal Ethics

The following information was supplied relating to ethical approvals (i.e., approving body and any reference numbers):

Our work did not involved experiments with living organisms. Only tissue collected from already dead individuals was used for DNA analyses. All DNA analyses are described in the “Methods” section.

DNA Deposition

The following information was supplied regarding the deposition of DNA sequences:

Sequences and respective haplotype frequencies for both mitochondrial DNA and MHC are available as Supplemental Information.

Data Availability

The following information was supplied regarding data availability:

We have provided the complete raw data, the above mentioned sequences and microsatellite allele frequencies as Supplemental Information.

Funding

MB-S is funded by the International Max Planck Research School for Evolutionary Biology. CE is partly supported by Deutsche Forschungsgemeinschaft grants (EI 841/4-1 and EI 841/6-1). This work was also supported by a research grant from the Fisheries Society of the British Isles. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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