Resource partitioning is not coupled with assortative mating in sympatrically divergent ricefish in a Wallacean ancient lake.

Oryzias Sulawesi digestive tract feeding morphology magic trait mate preference mating habitat sympatric speciation

Journal

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

Informations de publication

Date de publication:
07 2021
Historique:
revised: 07 04 2021
received: 09 01 2021
accepted: 25 05 2021
pubmed: 3 6 2021
medline: 15 12 2021
entrez: 2 6 2021
Statut: ppublish

Résumé

Sympatric speciation is considered to be difficult without the coupling between ecological traits that allow resource partitioning and reproductive traits that allow assortative mating. Such "magic traits" are known to be involved in most of the compelling examples of sympatric speciation. In this study, we report a possible case of sympatric speciation without magic traits. Three species of ricefish (genus Oryzias) are suggested to have diverged sympatrically within Lake Poso, an ancient lake in Sulawesi. An analysis of genome-wide single-nucleotide polymorphisms showed that these three species are reproductively isolated from each other throughout the lake. Stable isotope analyses revealed that the three species use different food resources, which reflect differences in their feeding morphologies (gill rakers and digestive tracts) and feeding sites. Field and laboratory observations showed that O. nebulosus and O. orthognathus share a mating habitat of cobbles, where they scatter fertilized eggs, whereas this site is never used by O. nigrimas, indicating that assortative mating is partly achieved by spatial isolation. The small, less-adhesive eggs of O. nebulosus and O. orthognathus probably reflect their adaptation to spawning on cobble beaches. Laboratory mating experiments showed strong prezygotic isolation between O. nebulosus and O. orthognathus, which is achieved by strong species recognition presumably by both sexes based on species-specific mating dances and nuptial coloration. In summary, the assortative mating of O. nebulosus and O. orthognathus is probably not coupled to resource partitioning. We discussed how sympatric speciation among these species might have been achieved even without magic traits.

Identifiants

pubmed: 34077583
doi: 10.1111/jeb.13874
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1133-1143

Informations de copyright

© 2021 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. https://doi.org/10.1101/gr.094052.109
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.
Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan Crater Lake cichlid fish. Nature, 439, 719-723. https://doi.org/10.1038/nature04325
Berlocher, S. H., & Feder, J. L. (2002). Sympatric speciation in phytophagous insects: Moving beyond controversy? Annual Review of Entomology, 47, 773-815. https://doi.org/10.1146/annurev.ento.47.091201.145312
Blake, R. W. (1983). Fish locomotion. Cambridge University Press.
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Bolnick, D. I., & Fitzpatrick, B. M. (2007). Sympatric speciation: Models and empirical evidence. Annual Review of Ecology, Evolution, and Systematics, 38, 459-487. https://doi.org/10.1146/annurev.ecolsys.38.091206.095804
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sinauer Associates.
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., & 1000 Genomes Project Analysis Group. (2011). The variant call format and VCFtools. Bioinformatics, 27, 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Dieckmann, U., & Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature, 400, 354-357. https://doi.org/10.1038/22521
Doebeli, M., Dieckmann, U., Metz, J. A. J., & Tautz, D. (2005). What we have also learned: Adaptive speciation is theoretically plausible. Evolution, 59, 691-695. https://doi.org/10.1554/04-154
Felsenstein, J. (1981). Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution, 35, 124-138. https://doi.org/10.1111/j.1558-5646.1981.tb04864.x
Foote, A. D. (2018). Sympatric speciation in the genomic era. Trends in Ecology & Evolution, 33, 85-95. https://doi.org/10.1016/j.tree.2017.11.003
Forbes, A. A., Powell, T. H. Q., Stelinski, L. L., Smith, J. J., & Feder, J. L. (2009). Sequential sympatric speciation across trophic levels. Science, 323, 776-779. https://doi.org/10.1126/science.1166981
Fujimoto, S., Miyake, T., & Yamahira, K. (2015). Latitudinal variation in male competitiveness and female choosiness in a fish: Are sexual selection pressures stronger at lower latitudes? Evolutionary Biology, 42, 75-87. https://doi.org/10.1007/s11692-014-9300-9
Futuyma, D. J., & Mayer, G. C. (1980). Non-allopatric speciation in animals. Systematic Zoology, 29, 254-271. https://doi.org/10.2307/2412661
German, D. P. (2011). Digestive efficiency. In A. P. Farrell (Ed.), Encyclopedia of fish physiology: From genome to environment (Vol. 3, pp. 1596-1607). Academic Press.
Giesen, W. (1994). Indonesia’s major freshwater lakes: A review of current knowledge, development processes and threats. Internationale Vereinigung für Theoretische und Angewandte Limnologie, 24, 115-128. https://doi.org/10.1080/05384680.1994.11904030
Hadid, Y., Pavlíček, T., Beiles, A., Ianovici, R., Raz, S., & Nevo, E. (2014). Sympatric incipient speciation of spiny mice Acomys at “Evolution Canyon,” Israel. Proceedings of the National Academy of Sciences of the United States of America, 111, 1043-1048.
Hadid, Y., Tzur, S., Pavlíček, T., Šumbera, R., Šklíba, J., Lövy, M., Fragman-Sapir, O., Beiles, A., Arieli, R., Raz, S., & Nevo, E. (2013). Possible incipient sympatric ecological speciation in blind mole rats (Spalax). Proceedings of the National Academy of Sciences of the United States of America, 110, 2587-2592.
Herder, F., Nolte, A. W., Pfaender, J., Schwarzer, J., Hadiaty, R. K., & Schliewen, U. K. (2006). Adaptive radiation and hybridization in Wallace’s Dreamponds: Evidence from sailfin silversides in the Malili Lakes of Sulawesi. Proceedings of the Royal Society B: Biological Sciences, 273, 2209-2217.
Higashi, M., Takimoto, G., & Yamamura, N. (1999). Sympatric speciation by sexual selection. Nature, 402, 523-526. https://doi.org/10.1038/990087
Iwamatsu, T. (2006). The integrated book for the biology of the medaka. Daigaku Kyouiku Publications. (in Japanese).
Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27, 3070-3071. https://doi.org/10.1093/bioinformatics/btr521
Kautt, A. F., Kratochwil, C. F., Nater, A., Machado-Schiaffino, G., Olave, M., Henning, F., Torres-Dowdall, J., Härer, A., Hulsey, C. D., Franchini, P., Pippel, M., Myers, E. W., & Meyer, A. (2020). Contrasting signatures of genomic divergence during sympatric speciation. Nature, 588, 106-111. https://doi.org/10.1038/s41586-020-2845-0
Kirkpatrick, M. (2001). Reinforcement during ecological speciation. Proceedings of the Royal Society B: Biological Sciences, 268, 1259-1263. https://doi.org/10.1098/rspb.2000.1427
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353-357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Kondrashov, A. S., & Kondrashov, F. A. (1999). Interactions among quantitative traits in the course of sympatric speciation. Nature, 400, 351-354. https://doi.org/10.1038/22514
Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. (2015). CLUMPAK: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179-1191.
Kopp, M., Servedio, M. R., Mendelson, T. C., Safran, R. J., Rodríguez, R. L., Hauber, M. E., Scordato, E. C., Symes, L. B., Balakrishnan, C. N., Zonana, D. M., & van Doorn, G. S. (2018). Mechanisms of assortative mating in speciation with gene flow: Connecting theory and empirical research. The American Naturalist, 191, 1-20. https://doi.org/10.1086/694889
Kottelat, M. (1990). The ricefishes (Oryziidae) of the Malili Lakes, Sulawesi, Indonesia, with description of a new species. Ichthyological Exploration of Freshwaters, 1, 151-166.
Langerhans, R. B., & Reznick, D. N. (2010). Ecology and evolution of swimming performance in fishes: Predicting evolution with biomechanics. In P. Domenici & B. G. Kapoor (Eds.), Fish locomotion: An eco-ethological perspective (pp. 200-248). Science Publishers.
Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27, 2987-2993. https://doi.org/10.1093/bioinformatics/btr509
Lunter, G., & Goodson, M. (2011). Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Research, 21, 936-939. https://doi.org/10.1101/gr.111120.110
Martin, C. H. (2013). Strong assortative mating by diet, color, size, and morphology but limited progress toward sympatric speciation in a classic example: Cameroon Crater Lake cichlids. Evolution, 67, 2114-2123. https://doi.org/10.1111/evo.12090
Martin, C. H., Cutler, J. S., Friel, J. P., Touokong, C. D., Coop, G., & Wainwright, P. C. (2015). Complex histories of repeated gene flow in Cameroon Crater Lake cichlids cast doubt on one of the clearest examples of sympatric speciation. Evolution, 69, 1406-1422. https://doi.org/10.1111/evo.12674
Mayr, E. (1963). Animal species and evolution. Belknap.
McCann, K. S., Rasmussen, J. B., & Umbanhowar, J. (2005). The dynamics of spatially coupled food webs. Ecology Letters, 8, 513-523. https://doi.org/10.1111/j.1461-0248.2005.00742.x
Mokodongan, D. F., Montenegro, J., Mochida, K., Fujimoto, S., Ishikawa, A., Kakioka, R., Yong, L., Mulis, Hadiaty, R. K., Mandagi, I. F., Masengi, K. W. A., Wachi, N., Hashiguchi, Y., Kitano, J., & Yamahira, K. (2018). Phylogenomics reveals habitat-associated body shape divergence in Oryzias woworae species group (Teleostei: Adrianichthyidae). Molecular Phylogenetics and Evolution, 118, 194-203. https://doi.org/10.1016/j.ympev.2017.10.005
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. https://doi.org/10.1007/s10228-003-0187-1
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. https://doi.org/10.1371/journal.pone.0037135
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Richards, E., Servedio, M., & Martin, C. (2019). Searching for sympatric speciation in the genomic era. BioEssays, 41, 1900047. https://doi.org/10.1002/bies.201900047
Rochette, N. C., Rivera-Colón, A. G., & Catchen, J. M. (2019). Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology, 28, 4737-4754. https://doi.org/10.1111/mec.15253
Savolainen, V., Anstett, M.-C., Lexer, C., Hutton, I., Clarkson, J. J., Norup, M. V., Powell, M. P., Springate, D., Salamin, N., & Baker, W. J. (2006). Sympatric speciation in palms on an oceanic island. Nature, 441, 210-213. https://doi.org/10.1038/nature04566
Schliewen, U. K., Tautz, D., & Paabo, S. (1994). Sympatric speciation suggested by monophyly of Crater Lake cichlids. Nature, 368, 629-632. https://doi.org/10.1038/368629a0
Servedio, M., & Noor, M. A. (2003). The role of reinforcement in speciation: Theory and data. Annual Review of Ecology, Evolution, and Systematics, 34, 339-364. https://doi.org/10.1146/annurev.ecolsys.34.011802.132412
Servedio, M. R., van Doorn, G. S., Kopp, M., Frame, A. M., & Nosil, P. (2011). Magic traits in speciation: “magic” but not rare? Trends in Ecology & Evolution, 26, 389-397. https://doi.org/10.1016/j.tree.2011.04.005
Sorenson, M. D., Sefc, K. M., & Payne, R. B. (2003). Speciation by host switch in brood parasitic indigobirds. Nature, 424, 928-931. https://doi.org/10.1038/nature01863
Sumarto, B. K. A., Nofrianto, A. B., Mokodongan, D. F., Lawelle, S. A., Masengi, K. W. A., Fujimoto, S., & Yamahira, K. (2021). Variation in mating behaviors between a tropical and a temperate species of medaka fishes. Zoological Science, 38, 45-50.
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. https://doi.org/10.1111/evo.13821
Tayasu, I., Hirasawa, R., Ogawa, N. O., Ohkouchi, N., & Yamada, K. (2011). New organic reference materials for carbon- and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. Limnology, 12, 261-266. https://doi.org/10.1007/s10201-011-0345-5
Via, S. (1999). Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution, 53, 1446-1457. https://doi.org/10.1111/j.1558-5646.1999.tb05409.x
von Rintelen, T., von Rintelen, K., Glaubrecht, M., Schubart, C. D., & Herder, F. (2012). Aquatic biodiversity hotspots in Wallacea: The species flocks in the ancient lakes of Sulawesi, Indonesia. In D. J. Gower, K. G. Johnson, J. E. Richardson, B. R. Rosen, L. Rüber, & S. T. Williams (Eds.), Biotic evolution and environmental change in southeast Asia (pp. 290-315). Cambridge University Press.
Webb, P. W. (1984). Body form, locomotion and foraging in aquatic vertebrates. American Zoologist, 24, 107-120. https://doi.org/10.1093/icb/24.1.107
Wootton, R. J. (1998). Ecology of teleost fishes (2nd ed.). Kluwer Academic Publishers.
Xu, J., Zhang, M., & Xie, P. (2011). Sympatric variability of isotope baselines influences modeling of fish trophic patterns. Limnology, 12, 107-115.

Auteurs

Ryo Kakioka (R)

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

Nobu Sutra (N)

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

Hirozumi Kobayashi (H)

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

Satoshi Ansai (S)

Graduate School of Life Sciences, Tohoku University, Sendai, Japan.

Kawilarang W A Masengi (KWA)

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

Atsushi J Nagano (AJ)

Faculty of Agriculture, Ryukoku University, Otsu, Japan.

Noboru Okuda (N)

Center for Ecological Research, Kyoto University, Shiga, Japan.

Rieko Tanaka (R)

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

Masahiro Sato (M)

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

Kazunori Yamahira (K)

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

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