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      Whole-Genome Sequencing of 84 Japanese Eels Reveals Evidence against Panmixia and Support for Sympatric Speciation

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          Abstract

          The Japanese eel ( Anguilla japonica), European eel ( Anguilla anguilla), and American eel ( Anguilla rostrata) are migratory, catadromous, temperate zone fish sharing several common life cycle features. The population genetics of panmixia in these eel species has already been investigated. Our extensive population genetics analysis was based on 1400 Gb of whole-genome sequence (WGS) data from 84 eels. It demonstrated that a Japanese eel group from the Kuma River differed from other populations of the same species. Even after removing the potential adapted/selected single nucleotide polymorphism (SNP) data, and with very small differences (fixation index [Fst] = 0.01), we obtained results consistently indicating that panmixia does not occur in Japanese eels. The life cycle of the Japanese eel is well-established and the Kuma River is in the center of its habitat. Nevertheless, simple reproductive isolation is not the probable cause of non-panmixia in this species. We propose that the combination of spawning area subdivision, philopatry, and habitat preference/avoidance accounts for the non-panmixia in the Japanese eel population. We named this hypothesis the “reproductive isolation like subset mapping” (RISM) model. This finding may be indicative of the initial stages of sympatric speciation in these eels.

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          The genomics of speciation-with-gene-flow.

          The emerging field of speciation genomics is advancing our understanding of the evolution of reproductive isolation from the individual gene to a whole-genome perspective. In this new view it is important to understand the conditions under which 'divergence hitchhiking' associated with the physical linkage of gene regions, versus 'genome hitchhiking' associated with reductions in genome-wide rates of gene flow caused by selection, can enhance speciation-with-gene-flow. We describe here a theory predicting four phases of speciation, defined by changes in the relative effectiveness of divergence and genome hitchhiking, and review empirical data in light of the theory. We outline future directions, emphasizing the need to couple next-generation sequencing with selection, transplant, functional genomics, and mapping studies. This will permit a natural history of speciation genomics that will help to elucidate the factors responsible for population divergence and the roles that genome structure and different forms of hitchhiking play in facilitating the genesis of new biodiversity. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            The genetic architecture of adaptation under migration-selection balance.

            Many ecologically important traits have a complex genetic basis, with the potential for mutations at many different genes to shape the phenotype. Even so, studies of local adaptation in heterogeneous environments sometimes find that just a few quantitative trait loci (QTL) of large effect can explain a large percentage of observed differences between phenotypically divergent populations. As high levels of gene flow can swamp divergence at weakly selected alleles, migration-selection-drift balance may play an important role in shaping the genetic architecture of local adaptation. Here, we use analytical approximations and individual-based simulations to explore how genetic architecture evolves when two populations connected by migration experience stabilizing selection toward different optima. In contrast to the exponential distribution of allele effect sizes expected under adaptation without migration (Orr 1998), we find that adaptation with migration tends to result in concentrated genetic architectures with fewer, larger, and more tightly linked divergent alleles. Even if many small alleles contribute to adaptation at the outset, they tend to be replaced by a few large alleles under prolonged bouts of stabilizing selection with migration. All else being equal, we also find that stronger selection can maintain linked clusters of locally adapted alleles over much greater map distances than weaker selection. The common empirical finding of QTL of large effect is shown to be expected with migration in a heterogeneous landscape, and these QTL may often be composed of several tightly linked alleles of smaller effect. © 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.
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              Extent and scale of local adaptation in salmonid fishes: review and meta-analysis.

              What is the extent and scale of local adaptation (LA)? How quickly does LA arise? And what is its underlying molecular basis? Our review and meta-analysis on salmonid fishes estimates the frequency of LA to be ∼55-70%, with local populations having a 1.2 times average fitness advantage relative to foreign populations or to their performance in new environments. Salmonid LA is evident at a variety of spatial scales (for example, few km to>1000 km) and can manifest itself quickly (6-30 generations). As the geographic scale between populations increases, LA is generally more frequent and stronger. Yet the extent of LA in salmonids does not appear to differ from that in other assessed taxa. Moreover, the frequency with which foreign salmonid populations outperform local populations (∼23-35%) suggests that drift, gene flow and plasticity often limit or mediate LA. The relatively few studies based on candidate gene and genomewide analyses have identified footprints of selection at both small and large geographical scales, likely reflecting the specific functional properties of loci and the associated selection regimes (for example, local niche partitioning, pathogens, parasites, photoperiodicity and seasonal timing). The molecular basis of LA in salmonids is still largely unknown, but differential expression at the same few genes is implicated in the convergent evolution of certain phenotypes. Collectively, future research will benefit from an integration of classical and molecular approaches to understand: (i) species differences and how they originate, (ii) variation in adaptation across scales, life stages, population sizes and environmental gradients, and (iii) evolutionary responses to human activities.
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                Author and article information

                Journal
                Genes (Basel)
                Genes (Basel)
                genes
                Genes
                MDPI
                2073-4425
                28 September 2018
                October 2018
                : 9
                : 10
                : 474
                Affiliations
                [1 ]Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan; aiga@ 123456mail.ecc.u-tokyo.ac.jp (Y.I.); schwarze.augen@ 123456aliyun.com (H.Z.); tanengkong@ 123456gmail.com (E.T.); akyoshita@ 123456g.ecc.u-tokyo.ac.jp (K.Y.); akino@ 123456mail.ecc.u-tokyo.ac.jp (S.K.); a-mituya@ 123456mail.ecc.u-tokyo.ac.jp (S.M.)
                [2 ]National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, Yokohama, Kanagawa 236-8648, Japan; sekino@ 123456affrc.go.jp (M.S.); chow@ 123456affrc.go.jp (S.C.); kobayash@ 123456fra.affrc.go.jp (T.K.); ksaitoh@ 123456affrc.go.jp (K.S.)
                [3 ]School of Marine Biosciences, Kitasato University, Sagamihara, Kanagawa 252-0373, Japan; yosinaga@ 123456kitasato-u.ac.jp (T.Y.); swatabe@ 123456kitasato-u.ac.jp (S.W.)
                [4 ]Yokosuka Laboratory, National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, Yokosuka, Kanagawa 238-0316, Japan; hkuro@ 123456affrc.go.jp (H.K.); toshiy@ 123456affrc.go.jp (T.Y.)
                [5 ]Department of Biology, Tokyo Medical University, Tokyo 160-8402, Japan; shinoda@ 123456tokyo-med.ac.jp
                [6 ]Institute of Fishery Science, College of Life Science, National Taiwan University, Taipei 10617, Taiwan; yshan@ 123456ntu.edu.tw
                [7 ]Bioresource Sciences, Faculty of Agriculture, Kyushu University, Fukuoka 812-0053, Japan; ryoshiro.wakiya@ 123456gmail.com (R.W.); mochioka@ 123456agr.kyushu-u.ac.jp (N.M.)
                [8 ]Minami-Izu Laboratory, National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, Kamo, Shizuoka 415-0156, Japan; h.kuwada@ 123456yutakanaumi.jp
                [9 ]Wakayama Prefectural Museum of Natural History, Kainan, Wakayama 642-0001, Japan; kaji_y0001@ 123456pref.wakayama.lg.jp
                [10 ]Department of Medical Genome Science, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa, Chiba 277-8561, Japan; ysuzuki@ 123456k.u-tokyo.ac.jp
                [11 ]Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan; tgojobor@ 123456nig.ac.jp
                Author notes
                [* ]Correspondence: asakawa@ 123456mail.ecc.u-tokyo.ac.jp ; Tel.: +81-3-5841-5296
                [†]

                Present address: National Association for the Promotion of Productive Seas, Kodenmacho Matsumura Bldg, Nihonbashi Kodenmacho, Chuo, Tokyo 103-0001, Japan.

                [‡]

                Present address: Tohoku National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Shiogama, Miyagi 985-0001, Japan.

                Author information
                https://orcid.org/0000-0002-3593-575X
                https://orcid.org/0000-0002-6458-1487
                https://orcid.org/0000-0001-7449-964X
                Article
                genes-09-00474
                10.3390/genes9100474
                6210723
                30274234
                d0f38a69-6103-494a-8208-d7f83b863c7e
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 03 August 2018
                : 21 September 2018
                Categories
                Article

                genome mapping,genetic patchiness,single nucleotide polymorphisms,population genomics,fixation index,endangered species

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