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Morphs Salvelinus Alpinus F1000Research 2016, 4:136 Last updated: 16 MAY 2019 RESEARCH ARTICLE The developmental transcriptome of contrasting Arctic charr (Salvelinus alpinus) morphs [version 3; peer review: 2 approved, 1 approved with reservations] Johannes Gudbrandsson1, Ehsan P. Ahi1, Sigridur R. Franzdottir1, Kalina H. Kapralova1, Bjarni K. Kristjansson2, S. Sophie Steinhaeuser1, Valerie H. Maier1, Isak M. Johannesson1, Sigurdur S. Snorrason1, Zophonias O. Jonsson1, Arnar Palsson1 1Institute of Life and Environmental Sciences, University of Iceland, Reykjavik, 101, Iceland 2Holar University College, Saudarkrokur, 551, Iceland First published: 01 Jun 2015, 4:136 ( Open Peer Review v3 https://doi.org/10.12688/f1000research.6402.1) Second version: 25 Apr 2016, 4:136 ( https://doi.org/10.12688/f1000research.6402.2) Reviewer Status Latest published: 02 Dec 2016, 4:136 ( https://doi.org/10.12688/f1000research.6402.3) Invited Reviewers 1 2 3 Abstract Species and populations with parallel evolution of specific traits can help illuminate how predictable adaptations and divergence are at the molecular version 3 report and developmental level. Following the last glacial period, dwarfism and published specialized bottom feeding morphology evolved rapidly in several 02 Dec 2016 landlocked Arctic charr Salvelinus alpinus populations in Iceland. To study the genetic divergence between small benthic morphs and limnetic morphs, we conducted RNA-sequencing charr embryos at four version 2 report report stages in early development. We studied two stocks with contrasting published morphologies: the small benthic (SB) charr from Lake Thingvallavatn and 25 Apr 2016 Holar aquaculture (AC) charr. The data reveal significant differences in expression of several biological version 1 pathways during charr development. There was also an expression published report report difference between SB- and AC-charr in genes involved in energy 01 Jun 2015 metabolism and blood coagulation genes. We confirmed differing expression of five genes in whole embryos with qPCR, including lysozyme 1 Daniel Macqueen, University of Aberdeen, and natterin-like which was previously identified as a fish-toxin of a lectin Aberdeen, UK family that may be a putative immunopeptide. We also verified differential expression of 7 genes in the developing head that associated consistently 2 Anne Dalziel, Laval University, Quebec City, with benthic v.s.limnetic morphology (studied in 4 morphs). Comparison of Canada single nucleotide polymorphism (SNP) frequencies reveals extensive genetic differentiation between the SB and AC-charr (~1300 with more than 3 Örjan Östman, Swedish University of 50% frequency difference). Curiously, three derived alleles in the otherwise Agricultural Sciences, Uppsala, Sweden conserved 12s and 16s mitochondrial ribosomal RNA genes are found in benthic charr. Any reports and responses or comments on the The data implicate multiple genes and molecular pathways in divergence of article can be found at the end of the article. small benthic charr and/or the response of aquaculture charr to domestication. Functional, genetic and population genetic studies on more Page 1 of 60 F1000Research 2016, 4:136 Last updated: 16 MAY 2019 domestication. Functional, genetic and population genetic studies on more freshwater and anadromous populations are needed to confirm the specific loci and mutations relating to specific ecological traits in Arctic charr. Keywords Salmonids, Aquaculture, ecomorphs, Polymorphism, parallel evolution, immunology, craniofacial divergence, mtDNA Corresponding authors: Johannes Gudbrandsson ([email protected]), Arnar Palsson ([email protected]) Competing interests: No competing interests were disclosed. Grant information: This project was supported by The Icelandic Center for Research (grant number: 100204011) to SSS, AP, ZOJ and BKK, The University of Iceland Research/Doctoral Fund to JG and KHK and University of Iceland research fund to AP, SSS and ZOJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2016 Gudbrandsson J et al. This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication). How to cite this article: Gudbrandsson J, Ahi EP, Franzdottir SR et al. The developmental transcriptome of contrasting Arctic charr ( Salvelinus alpinus) morphs [version 3; peer review: 2 approved, 1 approved with reservations] F1000Research 2016, 4:136 ( https://doi.org/10.12688/f1000research.6402.3) First published: 01 Jun 2015, 4:136 (https://doi.org/10.12688/f1000research.6402.1) Page 2 of 60 F1000Research 2016, 4:136 Last updated: 16 MAY 2019 One approach to identify pathways related to function or morpho- REVISED Amendments from Version 2 logical differences between species, populations or ecomorphs is 19,20 The changes to the manuscript are rewriting of the introduction, to study gene expression during development . For example a results and discussion to present more clearly the biology of microarray study of liver samples from anadromous and resident the Aquaculture charr used here as a reference strain, and the populations of brown trout (Salmo trutta), revealed that gene results from the contrast of the SB and AC transcriptomes and expression in juveniles was more influenced by life history than their implication both for evolutionary questions and also biology 21 22 of the AC-charr. We also set out to reduce the emphasis on the relatedness . Furthermore, Filteau et al. (2013) found a set of ecological divergence in the description and interpretation of coexpressed genes differentiating two whitefish morphotypes, the results. We also rewrote part of the introduction, to provide implicating Bone morphogenesis protein (BMP) signalling in the better flow from general to specific background, and shortened development of ecological differences in trophic morphology. the summary of molecular genetics of the craniofacial genes in the discussion. We clarified several issues, like the potential Thus we were quite keen to apply RNA-sequencing to analyse transgenerational effects in common garden experiment, the ecomorphs in Arctic charr. De novo assembly of genomes and description of the Salmonid ancestor genome duplication and the transcriptomes is complicated if many paralogs are present, age of the clade, and the qPCR results on both the Nattl genes which is the case in Arctic charr – see 23, 24. In this study we and the summary of validated genes. We amended Figure 1, opted for mapping the reads (36 bp) to a related reference genome/ Figure 2 and Figure 4, and cleaned or adjusted the language/ 25 spelling in accordance with the suggestions of the reviewers. We transcriptome , instead of de novo assembly. Two previous thank them dearly for their thoughtful comments and suggestions, studies have used RNA-seq to study salinity tolerance in adult which have clearly improved the manuscript. Arctic charr, and found links between gene expression and See referee reports quantitative trait loci23,24. Molecular studies of the highly polymorphic Arctic charr Following the end of the last glacial period, about 10.000 years Introduction ago, Arctic charr colonized northern freshwater systems26. It is Historical contingencies and chance shape organisms during found as anadromous or lake/stream residents and exhibits high evolution1,2, but convergence in phenotype and molecular systems level of within species polymorphism11,26. Charr is also known to indicates that evolution is to some extent predictable3,4. Identifi- harbour substantial phenotypic plasticity, which may promote or cation of genes and variants that influence evolved differences is reduce divergence9,27. Resource polymorphism in charr correlates not a trivial task5. Ideal systems to study the role of chance and with ecological attributes28–30. For instance small charr with benthic necessity in ecological evolution would be related species or morphology, are found in multiple lavaspring and stream habitats populations with readily observable phenotypic variation, living in Iceland31, and a comparative study of Icelandic lakes30 found in a tractable ecological setting, and showing parallel evolution that lakes with greater limnetic habitat, lower nutrients levels, of specific traits within/among species/populations. Examples of and greater potential for zooplankton consumption appeared to such species complexes are provided by finches of the Galapagos promote resource polymorphism. Some of the larger lakes con- islands6, while cichlids of the African great lakes also provide an tain two or more distinct morphs, typically limnetic and benthic exciting multi-species system in the same respect7. The threespine forms. Multiple lines of evidence show that these differences stickleback has also emerged as a model “single species” system8. stem both from environmental and genetic causes32–36. The best The amount of diversity in the feeding specializations of fish studied example of sympatric charr are the four morphs in Lake provide great opportunities for studying adaptation and divergence Thingvallavatn37; two have a benthic morphotype, a large ben- at the developmental and genetic level. thivorous (LB-charr) and a small benthivorous
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