Molecular ecology of the Javanese ricefish, Oryzias javanicus (Bleeker): genetic divergence along the Indonesian Archipelago
Eko Hardianto A * , Mio Hirayama B , Diah Permata Wijayanti C and Hideyuki Imai BA
B
C
Marine and Freshwater Research 74(15) 1314-1323 https://doi.org/10.1071/MF23129
Submitted: 6 July 2023 Accepted: 5 September 2023 Published: 22 September 2023
Abstract
Investigating the patterns of genetic diversity and population structure of the Javanese ricefish, Oryzias javanicus, is instrumental in identifying their dispersal patterns and demographics in response to ecological changes and biogeographical barriers.
To acquire a better understanding of the evolutionary history of Javanese ricefish.
We sequenced part of the mitochondrial DNA (mtDNA) control region in 335 individuals and genotyped 280 individuals for four microsatellite loci from seven Indonesian sites.
Both genetic diversity (h = 0.19–0.86 and DIVGene = 0.10–0.43) and nucleotide diversity (π = 0.06–0.61%) were low compared with other fish taxa. The analysis of molecular variance showed considerable genetic differences (P < 0.0001) for both genetic markers across all sampled locations. These results suggest that there has been a historical restriction on gene flow.
The observed population-structure pattern reflects a short pelagic larval development, which is closely linked to a restricted dispersal potential. This ultimately leads to isolation by distance, potentially allowing local adaptation to sites that augment any oceanographic, geographic, or biological barriers to gene flow.
The results presented in this study can be used to create more effective ways to protect the species in question.
Keywords: control region, gene flow, genetic diversity, Indonesia, Javanese ricefish, microsatellite, mitochondrial DNA, population structure.
References
Ackiss AS, Pardede S, Crandall E, Ablan-Lagman A, Ambariyanto A, Romena N, Barber PH, Carpenter KE (2013) Pronounced genetic structure in a highly mobile coral reef fish, Caesio cuning, in the Coral Triangle. Marine Ecology Progress Series 480, 185-197.
| Crossref | Google Scholar |
Arai T, Taha H (2021) Contrasting patterns of genetic population structure in tropical freshwater eels of genus Anguilla in the Indo-Pacific. Heliyon 7, e07097.
| Crossref | Google Scholar | PubMed |
Asahida T, Kobayashi T, Saitoh K, Nakayama I (1996) Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fisheries Science 62, 727-730.
| Crossref | Google Scholar |
Beck SV, Carvalho GR, Barlow A, Rüber L, Hui Tan H, Nugroho E, Wowor D, Mohd Nor SA, Herder F, Muchlisin ZA, de Bruyn M (2017) Plio-Pleistocene phylogeography of the Southeast Asian Blue Panchax killifish, Aplocheilus panchax. PLoS ONE 12, e0179557.
| Crossref | Google Scholar | PubMed |
Bleeker P (1854) Ichthyologische waarnemingen, gedaan op verschillende reizen in de residentie Banten. Natuurkundig Tijdschrift voor Nederlandische Indie 7, 309-326 [In Dutch].
| Google Scholar |
Bradbury IR, Laurel B, Snelgrove PVR, Bentzen P, Campana SE (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proceedings of the Royal Society of London – B. Biological Sciences 275, 1803-1809.
| Crossref | Google Scholar |
Carwenka AF, Brabdner J, Geist J, Schliewen UK (2014) Strong versus weak population genetic differentiation after a recent invasion of gobiid fishes (Neogobius melanostomus and Ponticola kessleri) in the upper Danube. Aquatic Invasions 9, 71-86.
| Crossref | Google Scholar |
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359-361.
| Crossref | Google Scholar |
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.
| Crossref | Google Scholar | PubMed |
Excoffier L, Lischer HEL (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.
| Crossref | Google Scholar |
Fitzpatrick JM, Carlon DB, Lippe C, Robertson DR (2011) The West Pacific diversity hotspot as a source or sink for new species? Population genetic insights from the Indo-Pacific parrotfish Scarus rubroviolaceus. Molecular Ecology 20, 219-234.
| Crossref | Google Scholar | PubMed |
Froukh T, Kochzius M (2007) Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea. Molecular Ecology 16, 1359-1367.
| Crossref | Google Scholar | PubMed |
Gotoh RO, Tamate S, Yokoyama J, Tamate HB, Hanzawa N (2013) Characterization of comparative genome-derived simple sequence repeats for acanthopterygian fishes. Molecular Ecology Resources 13(3), 461-472.
| Crossref | Google Scholar |
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485-486.
| Crossref | Google Scholar |
Grant WS, Bowen BW (2006) Living in a tilted world: climate change and geography limit speciation in Old World anchovies (Engraulis; Engraulidae). Biological Journal of the Linnean Society 88, 673-689.
| Crossref | Google Scholar |
Hardianto E, Wijayanti DP, Shy J-Y, Mather P, Hughes J, Imai H (2022a) Molecular ecology of the fiddler crab Austruca perplexa (H. Milne Edwards, 1852): genetic divergence along a major biogeographical barrier, Wallace’s Line. Biological Journal of the Linnean Society 135, 310-321.
| Crossref | Google Scholar |
Hardianto E, Fukuchi J, Hanamura Y, Wijayanti DP, Sabdono A, Imai H (2022b) Molecular ecology of a shallow water shrimp, Acetes sibogae sibogae Hansen 1919: evidence for strongly limited gene flow across the western Pacific. Marine Ecology 43, e12695.
| Crossref | Google Scholar |
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591-600.
| Google Scholar | PubMed |
Imai H, Cheng J-H, Hamasaki K, Numachi K-I (2004) Identification of four mud crab species (genus Scylla) using ITS-1 and 16S rDNA markers. Aquatic Living Resources 17, 31-34.
| Crossref | Google Scholar |
Iwamoto K, Chang C-W, Takemura A, Imai H (2012) Genetically structured population and demographic history of the goldlined spinefoot Siganus guttatus in the northwestern Pacific. Fisheries Science 78, 249-257.
| Crossref | Google Scholar |
Iwamoto K, Abdullah MF, Chang C-W, Yoshino T, Imai H (2015) Genetic isolation of the mottled spinefoot Siganus fuscescens Ryukyu Archipelago population. Biogeography 17, 61-85.
| Google Scholar |
Iwamoto K, Chang C-W, Imai H (2020) Spatial genetic structuring and demographic history of the little spinefoot Siganus spinus in the Western Pacific. Biogeography 22, 26-34.
| Google Scholar |
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801-1806.
| Crossref | Google Scholar | PubMed |
Janac M, Bryja J, Ondrackova M, Mendel J, Jurajda P (2017) Genetic structure of three invasive gobiid species along the Danube–Rhine invasion corridor: similar distributions, different histories. Aquatic Invansions 12, 551-564.
| Google Scholar |
Jombart T (2008) adegenet: an R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403-1405.
| Crossref | Google Scholar | PubMed |
Jombart T, Devillard S, Dufour A-B, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101, 92-103.
| Crossref | Google Scholar |
Kitada S, Nakajima K, Hamasaki K (2017) Population panmixia and demographic expansion of a highly piscivorous marine fish Scomberomorus niphonius. Journal of Fish Biology 91, 1435-1448.
| Crossref | Google Scholar | PubMed |
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15, 1179-1191.
| Crossref | Google Scholar | PubMed |
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547-1549.
| Crossref | Google Scholar | PubMed |
Kusuma WE, Ratmuangkhwang S, Kumazawa Y (2016) Molecular phylogeny and historical biogeography of the Indonesian freshwater fish Rasbora lateristriata species complex (Actinopterygii: Cyprinidae): cryptic species and west-to-east divergences. Molecular Phylogenetics and Evolution 105, 212-223.
| Crossref | Google Scholar |
LaRue EA, Ruetz CR, III, Stacey MB, Thum RA (2011) Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species. Hydrobiologia 663, 71-82.
| Crossref | Google Scholar |
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110-1116.
| Crossref | Google Scholar |
Liu S-YV, Kokita T, Dai C-F (2008) Population genetic structure of the neon damselfish (Pomacentrus coelestis) in the northwestern Pacific Ocean. Marine Biology 154, 745-753.
| Crossref | Google Scholar |
Lord C, Brun C, Hautecœur M, Keith P (2010) Comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobiidae: Sicydiinae) from Vanuatu and New Caledonia: insights on endemism. Ecology of Freshwater Fish 19, 26-38.
| Crossref | Google Scholar |
Mokodongan DF, Yamahira K (2015) Origin and intra-island diversification of Sulawesi endemic Adrianichthyidae. Molecular Phylogenetics and Evolution 93, 150-160.
| Crossref | Google Scholar |
Nuryanto A, Komalawati N, Sugiharto S (2019) Genetic diversity assessment of Hemibagrus nemurus from rivers in Java Island, Indonesia using COI gene. Biodiversitas 20, 2707-2717.
| Crossref | Google Scholar |
Parenti LR (2008) A phylogenetic analysis and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae). Zoological Journal of the Linnean Society 154, 494-610.
| Crossref | Google Scholar |
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90, 502-503.
| Crossref | Google Scholar |
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
| Crossref | Google Scholar | PubMed |
Raymond Jani Angel J, Vinay TN, Raghavan R, et al. (2019) First record of the Javanese ricefish, Oryzias javanicus (Bleeker, 1854) (Beloniformes: Adrianichthyidae) in the natural waters of India. Journal of Applied Ichthyology 35, 1034-1038.
| Crossref | Google Scholar |
Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105, 767-779.
| Crossref | Google Scholar | PubMed |
Rogers AR, Harpending H (1992) Population growth waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552-569.
| Google Scholar | PubMed |
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137-138.
| Crossref | Google Scholar |
Takehana Y, Zahm M, Cabau C, Klopp C, Roques C, Bouchez O, Donnadieu C, Barrachina C, Journot L, Kawaguchi M, Yasumasu S, Ansai S, Naruse K, Inoue K, Shinzato C, Schartl M, Guiguen Y, Herpin A (2020) Genome sequence of the euryhaline Javafish Medaka, Oryzias javanicus: a small aquarium fish model for studies on adaptation to salinity. G3 Genes|Genomes|Genetics 10, 907-915.
| Crossref | Google Scholar |
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512-526.
| Google Scholar | PubMed |
Termvidchakorn A, Magtoon W (2008) Development and identification of the ricefish Oryzias in Thailand. ScienceAsia 34, 416-423.
| Crossref | Google Scholar |
Tomita S, Matsuzaki S, Oka S-I, Toda M, Imai H (2016) 絶滅危惧種タナゴモドキ集団の高い遺伝的多様性と遺伝的均一性 [High levels of genetic diversity and gene flow in the endangered goby Hypseleotri cyprinoides on Okinawajima Island, Ishigakijima Island and Luzon Island.]. 魚類学雑誌 [Japanese Journal of Ichthyology] 63, 27-32 [In Japanese with English abstract].
| Crossref | Google Scholar |
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535-538.
| Crossref | Google Scholar |
Wainwright BJ, Arlyza IS, Karl SA (2018) Population genetics of the collector urchin, Tripneustes gratilla, in the Indonesian archipelago. Marine Ecology 39, e12530.
| Crossref | Google Scholar |
Wainwright BJ, Arlyza IS, Karl SA (2020a) Population genetic structure in the coral reef associated ascidian, Polycarpa aurata, throughout Wallacea, Indonesia. Regional Studies in Marine Science 39, 101430-101438.
| Crossref | Google Scholar |
Wainwright BJ, Arlyza IS, Karl SA (2020b) Population genetics of the banded coral shrimp, Stenopus hispidus (Olivier, 1811), in the Indonesian archipelago. Journal of Experimental Marine Biology and Ecology 525, 151325-151332.
| Crossref | Google Scholar |
Walter RP, Hogan JD, Haffner GD, Heath DD (2011) Genetic structure and connectivity among lake populations of threatened Paratherina sailfin silversides from Sulawesi, Indonesia. Conservation Genetics 12, 1387-1393.
| Crossref | Google Scholar |
Yusof S, Ismail A, Koito T, Kinoshita M, Inoue K (2012) Occurrence of two closely related ricefishes, Javanese medaka (Oryzias javanicus) and Indian medaka (O. dancena) at sites with different salinity in Peninsular Malaysia. Environmental Biology of Fishes 93, 43-49.
| Crossref | Google Scholar |
Yusoff NISM, Jaafar TNAM, Vilasri V, et al. (2021) Genetic diversity, population structure and historical demography of the two-spined yellowtail stargazer (Uranoscopus cognatus). Scientific Reports 11, 13357.
| Crossref | Google Scholar |
Zhao L, Wang S, Qu F, Liu Z, Gao T (2022) A genetic assessment of the population structure and demographic history of Odontamblyopus lacepedii (Perciformes, Amblyopinae) from the northwestern Pacific. ZooKeys 1088, 1-15.
| Crossref | Google Scholar | PubMed |