Ghost introgression in ricefishes of the genus Adrianichthys in an ancient Wallacean lake.

Sulawesi demography extinct lineage introgressive hybridization reproductive isolation secondary contact

Journal

Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954

Informations de publication

Date de publication:
10 2023
Historique:
revised: 06 07 2023
received: 11 05 2023
accepted: 01 08 2023
medline: 10 10 2023
pubmed: 22 9 2023
entrez: 22 9 2023
Statut: ppublish

Résumé

Because speciation might have been promoted by ancient introgression from an extinct lineage, it is important to detect the existence of 'ghost introgression' in focal taxa and examine its contribution to their diversification. In this study, we examined possible ghost introgression and its contributions to the diversification of ricefishes of the genus Adrianichthys in Lake Poso, an ancient lake on Sulawesi Island, in which some extinctions are known to have occurred. Population-genomic analysis revealed that two extant Adrianichthys species, A. oophorus and A. poptae are reproductively isolated from each other. Comparisons of demographic models demonstrated that introgression from a ghost population, which diverged from the common ancestor of A. oophorus and A. poptae, is essential for reconstructing the demographic history of Adrianichthys. The best model estimated that the divergence of the ghost population greatly predated the divergence between A. oophorus and A. poptae, and that the ghost population secondarily contacted the two extant species within Lake Poso more recently. Genome scans and simulations detected a greatly divergent locus, which cannot be explained without ghost introgression. This locus was also completely segregated between A. oophorus and A. poptae. These findings suggest that variants that came from a ghost population have contributed to the divergence between A. oophorus and A. poptae, but the large time-lag between their divergence and ghost introgression indicates that the contribution of introgression may be restricted.

Identifiants

pubmed: 37737547
doi: 10.1111/jeb.14223
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1484-1493

Informations de copyright

© 2023 European Society for Evolutionary Biology.

Références

Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655-1664.
Alonge, M., Soyk, S., Ramakrishnan, S., Wang, X., Goodwin, S., Sedlazeck, F. J., Lippman, Z. B., & Schatz, M. C. (2019). RaGOO: Fast and accurate reference-guided scaffolding of draft genomes. Genome Biology, 20, 224.
Ansai, S., Mochida, K., Fujimoto, S., Mokodongan, D. F., Sumarto, B. K. A., Masengi, K. W. A., Hadiaty, R. K., Nagano, A. J., Toyoda, A., Naruse, K., Yamahira, K., & Kitano, J. (2021). Genome editing reveals fitness effects of a gene for sexual dichromatism in Sulawesian fishes. Nature Communications, 12, 1350.
Ansai, S., Montenegro, J., Masengi, K. W. A., Nagano, A. J., Yamahira, K., & Kitano, K. (2022). Diversity of sex chromosomes in Sulawesian medaka fishes. Journal of Evolutionary Biology, 35, 1751-1764.
Barrier, M., Baldwin, B. G., Robichaux, R. H., & Purugganan, M. D. (1999). Interspecific hybrid ancestry of a plant adaptive radiation. Molecular Biology and Evolution, 16, 1105-1113.
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Dieckmann, U., & Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature, 400, 354-357.
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905.
Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10, 564-567.
Grant, P. R., & Grant, B. R. (2019). Hybridization increases population variation during adaptive radiation. Proceedings of the National Academy of Science of the United States of America, 116, 23216-23224.
Horoiwa, M., Mandagi, I. F., Sutra, N., Montenegro, J., Tantu, F. Y., Masengi, K. W. A., Nagano, A. J., Kusumi, J., Yasuda, N., & Yamahira, K. (2021). Mitochondrial introgression by ancient admixture between two distant lacustrine fishes in Sulawesi Island. PLoS One, 16, e0245316.
Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267.
Kakioka, R., Sutra, N., Kobayashi, H., Ansai, S., Masengi, K. W. A., Nagano, A. J., Okuda, N., Tanaka, R., Sato, M., & Yamahira, K. (2021). Resource partitioning is not coupled with assortative mating in sympatrically divergent ricefish in a Wallacean ancient lake. Journal of Evolutionary Biology, 34, 1133-1143.
Kottelat, M. (1990). Synopsis of the endangered buntingi (Osteichthyes: Adrianichthyidae and Oryziidae) of Lake Poso, Central Sulawesi, Indonesia, with a new reproductive guild and descriptions of three new species. Ichthyological Exploration of Freshwaters, 1, 49-67.
Li, H. (2018). Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics, 34, 3094-3100.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics, 25, 1754-1760.
Liu, S., Ferchaud, A. L., Grønkjaer, P., Nygaard, R., & Hansen, M. M. (2018). Genomic parallelism and lack thereof in contrasting systems of three-spined sticklebacks. Molecular Ecology, 27, 4725-4743.
Malinsky, M., Svardal, H., Tyers, A. M., Miska, E. A., Genner, M. J., Turner, G. F., & Durbin, R. (2018). Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nature Ecology & Evolution, 2, 1940-1955.
Mandagi, I. F., Kakioka, R., Montenegro, J., Kobayashi, H., Masengi, K. W. A., Inomata, N., Nagano, A. J., Toyoda, A., Ansai, S., Matsunami, M., Kimura, R., Kitano, J., Kusumi, J., & Yamahira, K. (2021). Species divergence and repeated ancient hybridization in a Sulawesian lake system. Journal of Evolutionary Biology, 34, 1767-1780.
Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A., & Zdobnov, E. M. (2021). BUSCO update: Novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Molecular Biology and Evolution, 38, 4647-4654.
Marques, D. A., Meier, J. I., & Seehausen, O. (2019). A combination view on speciation and adaptive radiation. Trends in Ecology & Evolution, 34, 531-544.
Meier, J. I., Marques, D. A., Mwaiko, S., Wagner, C. E., Excoffier, L., & Seehausen, O. (2017). Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nature Communications, 8, 14363.
Meier, J. I., Stelkens, R. B., Joyce, D. A., Mwaiko, S., Phiri, N., Schliewen, U. K., Selz, O. M., Wagner, C. E., Katongo, C., & Seehausen, O. (2019). The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlid fishes. Nature Communications, 10, 5391.
Mokodongan, D. F., & Yamahira, K. (2015). Origin and intra-Island diversification of Sulawesi endemic Adrianichthyidae. Molecular Phylogenetics and Evolution, 93, 150-160.
Montenegro, J., Fujimoto, S., Ansai, S., Nagano, A. J., Sato, M., Maeda, Y., Tanaka, R., Masengi, K. W. A., Kimura, R., Kitano, J., & Yamahira, K. (2022). Genetic basis for the evolution of pelvic-fin brooding, a new mode of reproduction, in a Sulawesian fish. Molecular Ecology, 31, 3798-3811.
Nei, M. (1972). Genetic distance between populations. American Naturalist, 106, 283-292.
Ottenburghs, J. (2020). Ghost introgression: Spooky gene flow in the distant past. BioEssays, 42, 2000012.
Parenti, L. R. (2008). A phylogenetic analyses and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae). Zoological Journal of the Linnean Society, 154, 494-610.
Parenti, L. R., & Soeroto, B. (2004). Adrianichthys roseni and Oryzias nebulosus, two new ricefishes (Atherinomorpha: Beloniformes: Adrianichthyidae) from Lake Poso, Sulawesi, Indonesia. Ichthyological Research, 51, 10-19.
Peterson, B. B. K., Weber, J. N. J., Kay, E. H. E., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest radseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7, e37135.
Poelstra, J. W., Richards, E. J., & Martin, C. H. (2018). Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids. Molecular Ecology, 27, 4270-4288.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 81, 559-575.
Richards, E. J., Servedio, M. R., & Martin, C. H. (2019). Searching for sympatric speciation in the genomic era. BioEssays, 41, 1900047.
Rieseberg, L. H., Kim, S. C., Randell, R. A., Whitney, K. D., Gross, B. L., Lexer, C., & Clay, K. (2007). Hybridization and the colonization of novel habitats by annual sunflowers. Genetica, 129, 149-165.
Rieseberg, L. H., Raymond, O., Rosenthal, D. M., Lai, Z., Livingstone, K., Nakazato, T., Durphy, J. L., Schwarzbach, A. E., Donovan, L. A., & Lexer, C. (2003). Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 29, 1211-1216.
Rochette, N., Rivera-Colón, A., & Catchen, J. (2019). Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology, 28, 4737-4754.
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sánchez-Gracia, A. (2017). DnaSP v6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution, 34, 3299-3302.
Schwarz, D., Matta, B. M., Shakir-Botteri, N. L., & McPheron, B. A. (2005). Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature, 436, 546-549.
Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198-207.
Selz, O. M., & Seehausen, O. (2019). Interspecific hybridization can generate functional novelty in cichlid fish. Proceedings of the Royal Society B: Biological Sciences, 286, 20191621.
Spivakov, M., Auer, T. O., Peravali, R., Dunham, I., Dolle, D., Fujiyama, A., Toyoda, A., Aizu, T., Minakuchi, Y., Loosli, F., Naruse, K., Birney, E., & Wittbrodt, J. (2014). Genomic and phenotypic characterization of a wild medaka population: Towards the establishment of an isogenic population genetic resource in fish. G3: Gene, Genomes, Genetics, 20, 433-445.
Sukamto, R. (2012). Geologic map of Indonesia, Ujung Pandang sheet. Ministry of Energy and Mineral Resources, Geological Agency.
Sun, Y., Abbott, R. J., Lu, Z., Mao, K., Zhang, L., Wang, X., Ru, D., & Liu, J. (2018). Reticulate evolution within a spruce (Picea) species complex revealed by population genomic analysis. Evolution, 72, 2669-2681.
Sutra, N., Kusumi, J., Montenegro, J., Kobayashi, H., Fujimoto, S., Masengi, K. W. A., Nagano, A. J., Toyoda, A., Matsunami, M., Kimura, R., & Yamahira, K. (2019). Evidence for sympatric speciation in a Wallacean ancient lake. Evolution, 73, 1898-1915.
van Doorn, G. S., & Weissing, F. J. (2002). Ecological versus sexual selection models of sympatric speciation: A synthesis. Selection, 2, 17-40.
von Rintelen, T., & Glaubrecht, M. (2006). Rapid evolution of sessility in an endemic species flock of the freshwater bivalve corbicula from ancient lakes on Sulawesi, Indonesia. Biology Letters, 2, 73-77.
von Rintelen, T., Wilson, A. B., Meyer, A., & Glaubrecht, M. (2004). Escalation and trophic specialization drive adaptive radiation of viviparous freshwater gastropods in the ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society B: Biological Sciences, 271, 2541-2549.
Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M., & Jaffe, D. B. (2017). Direct determination of diploid genome sequences. Genome Research, 27, 757-767.
Weissing, F. J., Edelaar, P., & van Doorn, G. S. (2011). Adaptive speciation theory: A conceptual review. Behavioral Ecology and Sociobiology, 65, 461-480.
Wilson, M. E., & Moss, S. J. (1999). Cenozoic paleogeographic evolution of Sulawesi and Borneo. Paleogeography, Paleoclimatology, Paleoecology, 145, 303-337.
Yamahira, K., Ansai, S., Kakioka, R., Yaguchi, H., Kon, T., Montenegro, J., Kobayashi, H., Fujimoto, S., Kimura, R., Takehana, Y., Setiamarga, D. H. E., Takami, Y., Tanaka, R., Maeda, K., Tran, H. D., Koizumi, N., Morioka, S., Bounsong, V., Watanabe, K., … Kitano, J. (2021). Mesozoic origin and ‘out-of-India’ radiation of ricefishes (Adrianichthyidae). Biology Letters, 17, 20210212.
Yao, Z., Long, S., Wang, C., Huang, C., Zhang, H., Jian, L., Huang, J., Guo, Y., Dong, Z., & Wang, Z. (2022). Population genetic characteristics of Hainan medaka with whole-genome resequencing. Frontiers in Genetics, 13, 946006.
Zheng, X., Levine, D., Shen, J., Gogarten, S. M., Laurie, C., & Weir, B. S. (2012). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28, 3326-3328.

Auteurs

Kazunori Yamahira (K)

Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan.

Hirozumi Kobayashi (H)

Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan.

Ryo Kakioka (R)

Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan.

Javier Montenegro (J)

Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan.

Kawilarang W A Masengi (KWA)

Faculty of Fisheries and Marine Science, Sam Ratulangi University, Manado, Indonesia.

Noboru Okuda (N)

Research Center for Inland Seas, Kobe University, Kobe, Japan.

Atsushi J Nagano (AJ)

Faculty of Agriculture, Ryukoku University, Otsu, Japan.
Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan.

Rieko Tanaka (R)

World Medaka Aquarium, Nagoya Higashiyama Zoo and Botanical Gardens, Nagoya, Japan.

Kiyoshi Naruse (K)

Laboratory of Bioresources, National Institute for Basic Biology, Okazaki, Japan.

Shoji Tatsumoto (S)

Cognitive Genomics Research Group, Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Japan.

Yasuhiro Go (Y)

Cognitive Genomics Research Group, Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Japan.
Department of System Neuroscience, Division of Behavioral Development, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Japan.
Department of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Hayama, Japan.

Satoshi Ansai (S)

Graduate School of Agriculture, Kyoto University, Kyoto, Japan.

Junko Kusumi (J)

Faculty of Social and Cultural Studies, Kyushu University, Fukuoka, Japan.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH