Reproductive isolation by time can occur in fish populations composed of individuals with different reproductive schedules. Most studies have tested this phenomenon using mature fish rather than their offspring, which may mask signals of population relationships.
We directly sampled fish eggs from artificial fish nests at four different time instances and subsequently fed the eggs to fish larvae in an indoor laboratory. Fish larvae, of each timeline, were randomly selected for species identification using the mitochondrial cytochrome c oxidase I (COI) gene and performed population analyses utilizing the concatenated sequences of COI gene and the mitochondrial control region (D-loop).
Neighbor-joining tree and Automatic Barcode Gap Discovery (ABGD) using COI sequences showed that all analyzed larvae can be assigned to the common carp (Cyprinus carpio). Significant differentiation among four demes inferred from the evidence of the concatenated sequences indicated temporal structuring in C. carpio demes within a reproductive season. Haplotype networks and a Bayesian method in BAPS also detected signals of population differentiation among the four demes.
The pattern observed in C. carpio demes revealed the reproductive strategy of the species and provided knowledge allowing establishment of conservation units.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
DNA sequences have been deposited in GenBank under Accession numbers MT089581–MT089602, MT089604–MT089622, MT089624–MT089703, MT093860–MT093985, and MW228494–MW228497. Details regarding individual samples are available in Table S1 and Table S2.
The nest material (Arundo donax) is a recycling plant species that have wide distributions.
Adámek Z, Anton Pardo M, Vilizzi L, Roberts J (2015) Successful reproduction of common carp Cyprinus carpio in irrigation waterways. Fisheries Manag Ecol 22(4):279–285
April J, Mayden RL, Hanner RH, Bernatchez L (2011) Genetic calibration of species diversity among North America’s freshwater fishes. Proc Natl Acad Sci USA 108(26):10602–10607
Balon EK (1995) Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129(1–4):3–48
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48
Barrett JC, Fry B, Maller J, Daly MJ (2004) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265
Braga-Silva A, Galetti PM (2016) Evidence of isolation by time in freshwater migratory fish Prochilodus costatus (Characiformes, Prochilodontidae). Hydrobiologia 765(1):159–167
Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163(1):367–374
Dudgeon D (2011) Asian river fishes in the anthropocene: threats and conservation challenges in an era of rapid environmental change. J Fish Biol 79(6):1487–1524
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567
Frantine-Silva W, Sofia S, Orsi M, Almeida F (2015) DNA barcoding of freshwater ichthyoplankton in the neotropics as a tool for ecological monitoring. Mol Ecol Resour 15(5):1226–1237
Hatanaka T, Henrique-Silva F, Galetti PM (2006) Population substructuring in a migratory freshwater fish Prochilodus argenteus (Characiformes, Prochilodontidae) from the São Francisco river. Genetics 126(1–2):153–159
Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270(1512):313–321
Hede Jørgensen HB, Hansen MM, Loeschcke V (2005) Spring-spawning herring (Clupea harengus L.) in the southwestern Baltic Sea: do they form genetically distinct spawning waves? ICES J Marine Sci 62(6):1065–1075
Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14(4):901–916
Huang B, Huang X (2011) Effects of two artificial fish nests on the soilless hydroculture of loach (Misgurnus anguillicaudatus). Aquaculture 5:1–3 (In Chinese)
Huang X, Zhao F, Song C, Gao Y, Geng Z, Zhuang P (2017) Effects of stereoscopic artificial floating wetlands on nekton abundance and biomass in the Yangtze Estuary. Chemosphere 183:510–518
Hubert N, Delrieu-Trottin E, Irisson JO, Meyer C, Planes S (2010) Identifying coral reef fish larvae through DNA barcoding: a test case with the families acanthuridae and holocentridae. Mol Phylogenet Evol 55(3):1195–1203
Hubert N, Espiau B, Meyer C, Planes S (2015) Identifying the ichthyoplankton of a coral reef using DNA barcodes. Mol Ecol Resour 15(1):57–67
Jeffries DL, Copp GH, Lawson Handley L, Olsén KH, Sayer CD, Hänfling B (2016) Comparing RAD seq and microsatellites to infer complex phylogeographic patterns, an empirical perspective in the Crucian carp, Carassius carassius. L Mol Ecol 25(13):2997–3018
Kimmerling N, Zuqert O, Amitai G, Gurevich T, Armoza-Zvuloni R, Kolesnikov I, Berenshtein I, Melamed S, Gilad S, Benjamin S, Rivlin A, Ohavia M, Paris CB, Holzman R, Kiflawi M, Sorek R (2018) Quantitative species-level ecology of reef fish larvae via metabarcoding. Nat Ecol Evol 2(2):306–316
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120
Kiss L, Pintye A, Kovacs GM, Jankovics T, Fontaine MC, Harvey N et al. (2011) Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Mol Ecol 20(7):1492–1507
Ko HL, Wang YT, Chiu TS, Lee MA, Leu MY, Chang KZ et al (2013) Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8(1):e53451
Li T, Liu Z, Zheng Q, He T, Liu J (2019) Effect evaluation of artificial fish nest in Beibei section of Jialing river. Freshw Fish 49(1):57–61
Li Y, Chen W, Xia Y, Yang J, Zhu S, Li X (2020) Materials selection and influencing factors analysis of artificial fish nest implementation. South China Fisheries Sci 16(2):21–28
Li Y, Guo M, Zhan C, Yang X, Dong Y (2016) The enhancement effects of fishery resources on artificial fish nest: a review. Freshw Fish 48(4):58–62
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452
McPherson AA, Stephenson RL, Taggart CT (2003) Genetically different Atlantic herring Clupea harengus spawning waves. Mar Ecol Prog Ser 247:303–309
Møller A, Antonov A, Stokke B, Fossøy F, Moksnes A, Røskaft E, Takasu F (2011) Isolation by time and habitat and coexistence of distinct host races of the common cuckoo. J Evol Biol 24(3):676–684
Pan P, Li Y, Li X (2016) Effect evaluation of artificial fishnest on common carp ( Cyprinus carpio) in Xijiang river. Freshw Fish 46(6):45–49
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877
Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20(9):1952–1963
Santos LN, Agostinho AA, Alcaraz C, Carol J, Santos AF, Tedesco P, García-Berthou E (2011) Artificial macrophytes as fish habitat in a Mediterranean reservoir subjected to seasonal water level disturbances. Aquat Sci 73(1):43–52
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690
Smith BB, Walker K (2004) Spawning dynamics of common carp in the river Murray, South Australia, shown by macroscopic and histological staging of gonads. J Fish Biol 64(2):336–354
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Tan X, Li X, Lin J, Li Y, Bi Y, Li J, Wang C (2009) Early morphogenesis and larval resources of common carp at Zhaoqing section in the Pearl River. J Dalian Ocean Univ 24(2):125–129 (In Chinese)
Uzunova EP, Studenkov S, Simeonovska-Nikolova D (2014) A field study on using artificial substrate for nesting of introduced pumpkinseed sunfish, Lepomis gibbosus (Linnaeus, 1758). Anim Biol 64(1):115–124
Valdez-Moreno M, Vásquez-Yeomans L, Elías-Gutiérrez M, Ivanova NV, Hebert PD (2010) Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management. Mar Freshw Res 61(6):655–671
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277(5325):494–499
Wang C, Li S, Nagy ZT, Lehoczky I, Huang L, Zhao Y, Song X, Jeney Z (2010) Molecular genetic structure and relationship of Chinese and Hungarian common carp (Cyprinus carpio L.) strains based on mitochondrial sequence. Aquac Res 41(9):1339–1347
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PD (2005) DNA barcoding Australia’s fish species. Philo T R S B 360(1462):1847–1857
Wohlfarth GW (1993) Heterosis for growth rate in common carp. Aquaculture 113(1-2):31–46
Yang Z (1981) Artificial propagation of Cyprinus carpio during three seasons. Freshw Fish 1:31–32 (In Chinese)
Yang JX, Pan XF, Chen XY, Wang XA, Zhao YP, Li JY, Li ZY (2013) Overview of the artificial enhancement and release of endemic freshwater fish in China. Zool Res 34(4):267–280
Zhou J, Zhang C (2005) Freshwater fishes of Guangxi, China. Guangxi People’s Publishing House, Nanning, China
Zu G, Wang D, Li A (1985) Preliminary report of the effect of large-scale artificial fish nest proliferation in Xianghongdian reservoir. Reserv Fish 4:45–47
We are grateful to Maochuan Ao for assistances in collecting specimens.
This research was supported by National Key R&D Program of China (2018YFD0900903) and Central Public-interest Scientific Institution Basal Research Fund, CAFS (2017HY-ZD0103).
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval and consent to participate
All experimental protocols were approved by the Ethics Committee of the Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science. Te policies were enacted according to Chinese Association for Laboratory Animal Sciences, and coordinated with the Institutional Animal Care and Use Committee (IACUC) protocols (http://iacuc.usc.edu/).
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Below is the link to the electronic supplementary material.
About this article
Cite this article
Chen, W., Zhu, S., Li, X. et al. Molecular identification and temporal genetic differentiation of Cyprinus carpio (Cypriniformes: Cyprinidae) eggs attached on artificial fish nests. Conservation Genet Resour (2021). https://doi.org/10.1007/s12686-021-01189-5
- Cyprinus carpio
- DNA barcodes
- Temporal differentiation
- Fish eggs and larvae
- Artificial fish nest