Genomic signatures for latitudinal selection in the tropical eel Anguilla marmorata.
ecological niche
eel
panmixia
whole-genome sequencing
within-generation selection
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
11
02
2022
received:
26
08
2021
accepted:
14
02
2022
pubmed:
25
3
2022
medline:
12
5
2022
entrez:
24
3
2022
Statut:
ppublish
Résumé
Selection acting across environmental gradients, such as latitudes, can cause spatial structuring of genomic variants even within panmictic populations. In this study, we focused on the within-generation latitudinal selection between northernmost and southernmost individuals of the North Pacific population of a tropical eel Anguilla marmorata, which shares its northernmost distribution with a temperate eel Anguilla japonica. Whole-genome sequencing data indicated that the northernmost and southernmost individuals of A. marmorata belong to a single panmictic population, as suggested by previous studies. On the contrary, parts of genomic regions across multiple chromosomes exhibited significant genetic differentiation between the northernmost and southernmost individuals, and in these genomic regions, the genotypes of the northernmost individuals were similar to those of A. japonica. These findings suggested within-generation latitudinal selection of A. marmorata, which might have led to genetic closeness between northernmost A. marmorata and A. japonica.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
763-771Subventions
Organisme : KAKENHI
ID : JP17H03859
Informations de copyright
© 2022 European Society for Evolutionary Biology.
Références
Alexander, D. H., & Lange, K. (2011). Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics, 12, 246. https://doi.org/10.1186/1471-2105-12-246
Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655-1664. https://doi.org/10.1101/gr.094052.109
Anacker, B.L., & Strauss, S. Y. (2014). The geography and ecology of plant speciation: range overlap and niche divergence in sister species. Proceedings of the Royal Society B: Biological Sciences, 281, 20132980. https://doi.org/10.1098/rspb.2013.2980
Babin, C., Gagnaire, P. A., Pavey, S. A., & Bernatchez, L. (2017). RAD-seq reveals patterns of additive polygenic variation caused by spatially-varying selection in the American eel (Anguilla rostrata). Genome Biology and Evolution, 9, 2974-2986. https://doi.org/10.1093/gbe/evx226
Barth, J. M. I., Gubili, C., Matschiner, M., Tørresen, O. K., Watanabe, S., Egger, B., Han, Y.-S., Feunteun, E., Sommaruga, R., Jehle, R., & Schabetsberger, R. (2020). Stable species boundaries despite ten million years of hybridization in tropical eels. Nature Communications, 11, 1-13. https://doi.org/10.1038/s41467-020-15099-x
Bonhomme, M., Chevalet, C., Servin, B., Boitard, S., Abdallah, J., Blott, S., & SanCristobal, M. (2010). Detecting selection in population trees: The Lewontin and Krakauer test extended. Genetics, 186, 241-262. https://doi.org/10.1534/genetics.110.117275
Castle, P. H. J., & Williamson, G. R. (1974). On the validity of the fresh-water eel species Anguilla ancestralis Ege, from Celebes. Copeia, 2, 569-570.
Cayuela, H., Rougemont, Q., Laporte, M., Mérot, C., Normandeau, E., Dorant, Y., Tørresen, O. K., Hoff, S. N. K., Jentoft, S., Sirois, P., Castonguay, M., Jansen, T., Praebel, K., Clément, M., & Bernatchez, L. (2020). Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish. Molecular Ecology, 29, 2379-2398. https://doi.org/10.1111/mec.15499
Chang, Y.-L.-K., Feunteun, F., Miyazawa, Y., & Tsukamoto, K. (2020). New clues on the Atlantic eels spawning behavior and area: The Mid-Atlantic Ridge hypothesis. Scientific Reports, 10, e15981. https://doi.org/10.1038/s41598-020-72916-5
Chang, Y.-L.-K., Miller, M. J., Tsukamoto, K., & Miyazawa, Y. (2018). Effect of larval swimming in the western North Pacific subtropical gyre on the recruitment success of the Japanese eel. PLoS One, 13, e0208704. https://doi.org/10.1371/journal.pone.0208704
Chen, Y., Chen, Y., Shi, C., Huang, Z., Zhang, Y., Li, S., Li, Y., Ye, J., Yu, C., Li, Z., Zhang, X., Wang, J., Yang, H., Fang, L., & Chen, Q. (2018). SOAPnuke: A MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience, 7, gix120. https://doi.org/10.1093/gigascience/gix120
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., & Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics, 27, 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Davis, M. B., & Shaw, R. G. (2001). Range shifts and adaptive responses to quaternary climate change. Science, 292, 673-679. https://doi.org/10.1126/science.292.5517.673
Ege, V. A. (1939). A revision of the genus Anguilla Shaw: A systematic, phylogenetic and geographical study. Dana Report, 16, 1-256.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fraser, D. J., Weir, L. K., Bernatchez, L., Hansen, M. M., & Taylor, E. B. (2011). Extent and scale of local adaptation in salmonid fishes: Review and meta-analysis. Heredity, 106, 404-420. https://doi.org/10.1038/hdy.2010.167
Gagnaire, P. A., Minegishi, Y., Zenboudji, S., Valade, P., Aoyama, J., & Berrebi, P. (2011). Within-population structure highlighted by differential introgression across semipermeable barriers to gene flow in Anguilla marmorata. Evolution, 65, 3413-3427. https://doi.org/10.1111/j.1558-5646.2011.01404.x
Gagnaire, P. A., Normandeau, E., Côté, C., Møller Hansen, M., & Bernatchez, L. (2012). The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics, 190, 725-736. https://doi.org/10.1534/genetics.111.134825
Griffin, E. A. Jr, Staknis, D., & Weitz, C. J. (1999). Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science, 286, 768-771. https://doi.org/10.1126/science.286.5440.768
Günther, A., Einwich, A., Sjulstok, E., Feederle, R., Bolte, P., Koch, K. W., Solov'yov, I. A., & Mouritsen, H. (2018). Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4. Current Biology, 28, 211-223.e4. https://doi.org/10.1016/j.cub.2017.12.003
Hagihara, S., Aoyama, J., Limbong, D., & Tsukamoto, K. (2012). Morphological and physiological changes of female tropical eels, Anguilla celebesensis and Anguilla marmorata, in relation to downstream migration. Journal of Fish Biology, 81, 408-426. https://doi.org/10.1111/j.1095-8649.2012.03332.x
Hagihara, S., Aoyama, J., Limbong, D., & Tsukamoto, K. (2018). Age and growth of migrating tropical eels, Anguilla celebesensis and Anguilla marmorata. Journal of Fish Biology, 92, 1526-1544. https://doi.org/10.1111/jfb.13608
Halbritter, A. H., Billeter, R., Edwards, P. J., & Alexander, J. M. (2015). Local adaptation at range edges: Comparing elevation and latitudinal gradients. Journal of Evolutionary Biology, 28, 1849-1860. https://doi.org/10.1111/jeb.12701
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009a). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37, 1-13. https://doi.org/10.1093/nar/gkn923
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009b). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44-57. https://doi.org/10.1038/nprot.2008.211
Igarashi, Y., Zhang, H., Tan, E., Sekino, M., Yoshitake, K., Kinoshita, S., Mitsuyama, S., Yoshinaga, T., Chow, S., Kurogi, H., Shinoda, A., Han, Y.-S., Wakiya, R., Mochioka, N., Yamamoto, T., Kuwada, H., Kaji, Y., Suzuki, Y., Gojobori, T., … Asakawa, S. (2018). Whole-genome sequencing of 84 Japanese eels reveals evidence against panmixia and support for sympatric speciation. Genes, 9, 474. https://doi.org/10.3390/genes9100474
Ishikawa, S., Tsukamoto, K., & Nishida, M. (2004). Genetic evidence for multiple geographic populations of the giant mottled eel Anguilla marmorata in the Pacific and Indian oceans. Ichthyological Research, 51, 343-353. https://doi.org/10.1007/s10228-004-0241-7
Kim, D., Paggi, J. M., Park, C., Bennett, C., & Salzberg, S. L. (2019). Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907-915. https://doi.org/10.1038/s41587-019-0201-4
Kovaka, S., Zimin, A. V., Pertea, G. M., Razaghi, R., Salzberg, S. L., & Pertea, M. (2019). Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biology, 20, 1-13. https://doi.org/10.1186/s13059-019-1910-1
Kumai, K., Kuroki, M., & Morita, K. (2021). Influence of environmental parameters on habitat use by sympatric freshwater eels Anguilla marmorata and Anguilla japonica on Yakushima Island, Japan. Canadian Journal of Zoology, 99, 1020-1027. https://doi.org/10.1139/cjz-2021-0125
Kumai, Y., Tsukamoto, K., & Kuroki, M. (2020). Growth and habitat use of two anguillid eels, Anguilla marmorata and A. japonica, on Yakushima Island, Japan. Ichthyological Research, 67, 375-384. https://doi.org/10.1007/s10228-020-00732-y
Kuroki, M., Aoyama, J., Miller, M., Yoshinaga, T., Shinoda, A., Hagihara, S., & Tsukamoto, K. (2009). Sympatric spawning of Anguilla marmorata and Anguilla japonica in the western North Pacific Ocean. Journal of Fish Biology, 74, 1853-1865. https://doi.org/10.1111/j.1095-8649.2009.02299.x
Kuroki, M., Miller, M. J., & Tsukamoto, K. (2014). Diversity of early life-history traits in freshwater eels and the evolution of their oceanic migrations. Canadian Journal of Zoology, 92, 749-770. https://doi.org/10.1139/cjz-2013-0303
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
Luu, K., Bazin, E., & Blum, M. G. (2017). pcadapt: An R package to perform genome scans for selection based on principal component analysis. Molecular Ecology Resources, 17, 67-77. https://doi.org/10.1111/1755-0998.12592
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., & DePristo, M. A. (2010). The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297-1303. https://doi.org/10.1101/gr.107524.110
Meirmans, P. G., & Van Tienderen, P. H. (2004). GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4, 792-794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Miller, M. J., & Tsukamoto, K. (2017). The ecology of oceanic dispersal and survival of anguillid leptocephali. Canadian Journal of Fisheries and Aquatic Sciences, 74, 958-971. https://doi.org/10.1139/cjfas-2016-0281
Minegishi, Y., Aoyama, J., & Tsukamoto, K. (2008). Multiple population structure of the giant mottled eel, Anguilla marmorata. Molecular Ecology, 17, 3109-3122. https://doi.org/10.1111/j.1365-294X.2008.03822.x
Naisbett-Jones, L. C., Putman, N. F., Stephenson, J. F., Ladak, S., & Young, K. A. (2017). A magnetic map leads Juvenile European Eels to the Gulf Stream. Current Biology, 27, 1236-1240. https://doi.org/10.1016/j.cub.2017.03.015
Pavey, S. A., Gaudin, J., Normandeau, E., Dionne, M., Castonguay, M., Audet, C., & Bernatchez, L. (2015). RAD sequencing highlights polygenic discrimination of habitat ecotypes in the panmictic American eel. Current Biology, 25, 1666-1671. https://doi.org/10.1016/j.cub.2015.04.062
Pritchard, J. K., Matthew, S., & Peter, D. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. https://doi.org/10.1093/genetics/155.2.945
Pujolar, J. M., Jacobsen, M., Als, T. D., Frydenberg, J., Magnussen, E., Jónsson, B., Jiang, X., Cheng, L., Bekkevold, D., Maes, G., Bernatchez, L., & Hansen, M. (2014). Assessing patterns of hybridization between North Atlantic eels using diagnostic single-nucleotide polymorphisms. Heredity, 112, 627-637. https://doi.org/10.1038/hdy.2013.145
Pujolar, J. M., Jacobsen, M. W., Als, T. D., Frydenberg, J., Munch, K., Jónsson, B., Jian, J. B., Cheng, L., Maes, G. E., Bernatchez, L., & Hansen, M. M. (2014). Genome-wide single-generation signatures of local selection in the panmictic European eel. Molecular Ecology, 23, 2514-2528. https://doi.org/10.1111/mec.12753
Quinlan, A. R., & Hall, I. M. (2010). BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842. https://doi.org/10.1093/bioinformatics/btq033
Rhie, A., McCarthy, S.A., Fedrigo, O., Damas, J., Formenti, G., Koren, S., Uliano-Silva, M., Chow, W., Fungtammasan, A., Kim, J., Lee, C., Ko, B.J., Chaisson, M., Gedman, G. L., Cantin, L. J., Thibaud-Nissen, F., Haggerty, L., Bista, I., Smith, M., … Jarvis, E.D. (2021). Towards complete and error-free genome assemblies of all vertebrate species. Nature, 592, 737-746. https://doi.org/10.1038/s41586-021-03451-0.
Roesti, M., Gavrilets, S., Hendry, A. P., Salzburger, W., & Berner, D. (2014). The genomic signature of parallel adaptation from shared genetic variation. Molecular Ecology, 23, 3944-3956. https://doi.org/10.1111/mec.12720
Savolainen, O., Lascoux, M., & Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics, 14, 807-820. https://doi.org/10.1038/nrg3522
Tesch, F. W. (2003). The eel, 3rd ed. Blackwell Science Ltd.
Ulrik, M. G., Pujolar, J. M., Ferchaud, A.-L., Jacobsen, M. W., Als, T. D., Gagnaire, P. A., Frydenberg, J., Bøcher, P. K., Jónsson, B., Bernatchez, L., & Hansen, M. M. (2014). Do North Atlantic eels show parallel patterns of spatially varying selection? BMC Evolutionary Biology, 14, 1-11. https://doi.org/10.1186/1471-2148-14-138
Wakiya, R., Itakura, H., & Kaifu, K. (2019). Age, growth, and sex ratios of the giant mottled eel, Anguilla marmorata, in freshwater habitats near its northern geographic limit: A comparison to tropical regions. Zoological Studies, 58, e34. https://doi.org/10.6620/ZS.2019.58-34
Watanabe, S., Aoyama, J., & Tsukamoto, K. (2004). Reexamination of Ege's (1939) use of taxonomic characters of the genus Anguilla. Bulletin of Marine Science, 74, 337-351.
Watanabe, S., Aoyama, J., & Tsukamoto, K. (2009). A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fisheries Science, 75, 387-392. https://doi.org/10.1007/s12562-009-0087-z
Watanabe, S., Miller, M., Aoyama, J., & Tsukamoto, K. (2009). Morphological and meristic evaluation of the population structure of Anguilla marmorata across its range. Journal of Fish Biology, 74, 2069-2093. https://doi.org/10.1111/j.1095-8649.2009.02297.x
Whitlock, M. C., & Lotterhos, K. E. (2015). Reliable detection of loci responsible for local adaptation: Inference of a null model through trimming the distribution of FST. The American Naturalist, 186, S24-S36. https://doi.org/10.1086/682949
Willig, M. R., Kaufman, D. M., & Stevens, R. D. (2003). Latitudinal gradients of biodiversity: Pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics, 34, 273-309. https://doi.org/10.1146/annurev.ecolsys.34.012103.144032
Xu, J., Jarocha, L. E., Zollitsch, T., Konowalczyk, M., Henbest, K. B., Richert, S., Golesworthy, M. J., Schmidt, J., Déjean, V., Sowood, D. J. C., Bassetto, M., Luo, J., Walton, J. R., Fleming, J., Wei, Y., Pitcher, T. L., Moise, G., Herrmann, M., Yin, H., … Hore, P. J. (2021). Magnetic sensitivity of cryptochrome 4 from a migratory songbird. Nature, 594, 535-540. https://doi.org/10.1038/s41586-021-03618-9
Zhou, Y., Duvaux, L., Ren, G., Zhang, L., Savolainen, O., & Liu, J. (2017). Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions. Heredity, 118, 211-220. https://doi.org/10.1038/hdy.2016.72