Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Polygamy and low effective population size in a captive Murray cod (Maccullochella peelii peelii) population: genetic implications for wild restocking programs

Meaghan L. Rourke A B D F , Helen C. McPartlan B E , Brett A. Ingram C and Andrea C. Taylor A

A Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

B Primary Industries Research Victoria, Department of Primary Industries, Attwood, Vic. 3049, Australia.

C Primary Industries Research Victoria, Department of Primary Industries, Alexandra, Vic. 3714, Australia.

D Present address: Narrandera Fisheries Centre, NSW Department of Primary Industries, Narrandera, NSW 2700, Australia.

E Present address: Primary Care Research Unit, Department of General Practice, University of Melbourne, Carlton, Vic. 3053, Australia.

F Corresponding author. Email: meaghan.rourke@dpi.nsw.gov.au

Marine and Freshwater Research 60(8) 873-883 https://doi.org/10.1071/MF08218
Submitted: 25 July 2008  Accepted: 21 February 2009   Published: 27 August 2009

Abstract

Stocking of freshwater fish species with hatchery-bred fish is a common response to depleted wild stocks, but may have numerous genetic implications. Murray cod, Maccullochella peelii peelii (Mitchell), have been produced in captivity for wild stocking programs for more than 30 years. The potential genetic impacts of this stocking program on wild populations was investigated by using eight microsatellite markers to determine the parentage of 1380 offspring from 46 separate spawnings collected over three consecutive breeding seasons, and by estimating the effective population size of the broodfish generation through demographic and genetic methods. Results revealed unexpected incidences of polygamous spawnings (both polygyny and polyandry), multiple spawnings by both sexes within a season and repeated matings between pairs of fish across multiple seasons. Furthermore, approximately half of the broodfish failed to spawn at all over the 3-year study period. This likely contributed to the estimated effective population size of around half of the census size, moderate but significant reductions in allelic richness in all three cohorts investigated and a small but significant reduction in heterozygosity in two cohorts. These results allowed us to make recommendations regarding captive husbandry that will maximise genetic diversity of fish intended for stocking.

Additional keywords: microsatellite, parentage analysis, stocking.


Acknowledgements

We sincerely thank the Animal Genetics and Genomics Platform of Primary Industries Research Victoria, where most laboratory work and data analyses were conducted. We also thank the staff of Snobs Creek Hatchery for assisting with sampling and two anonymous reviewers for their valuable comments. The Victorian Government’s Our Rural Landscape Initiative, Fisheries Victoria and the Holsthworth Wildlife Research Fund provided funding for the project. Meaghan Rourke was supported by an Australian Postgraduate Award through Monash University. The research was conducted under animal ethics approvals from the Department of Primary Industries (AEC Fish Nov 05 0001) and Monash University (BSCI/2005/02).


References

Allendorf, F. W. (1993). Delay of adaptation to captive breeding by equalizing family size. Conservation Biology 7, 416–419.
CrossRef |

Ardren, W. R. , and Kapuscinski, A. R. (2003). Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout. Molecular Ecology 12, 35–49.
CrossRef | CAS | PubMed |

Bartley, D. , Bagley, M. , Gall, G. , and Bentley, B. (1992). Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conservation Biology 6, 365–375.
CrossRef |

Bekkevold, D. , Hansen, M. M. , and Loeschcke, V. (2002). Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.). Molecular Ecology 11, 91–102.
CrossRef | CAS | PubMed |

Borrell, Y. J. , Álvarez, J. , Vázquez, E. , Pato, C. F. , Tapia, C. M. , Sánchez, J. A. , and Blanco, G (2004). Applying microsatellites to the management of farmed turbot stocks (Scophthalmus maximus L.) in hatcheries. Aquaculture 241, 133–150.
CrossRef | CAS |

Cadwallader P. L. (1977). J. O. Langtry’s 1949–50 Murray River investigations. Fisheries and Wildlife Division, Victoria, Number 13.

Cowx, I. G. (1999). An appraisal of stocking strategies in the light of developing country constraints. Fisheries Management and Ecology 6, 21–34.
CrossRef |

Crow J. F., and Kimura M. (1970). ‘An Introduction to Population Genetics Theory.’ (Harper and Row: New York.)

Dakin, W. J. , and Kesteven, G. L. (1938). The Murray Cod (Maccullochella macquariensis (Cuv. et Val.). Some experiments on breeding with notes on the early stages and a reference to the problems of depletion and restocking. New South Wales State Fisheries Research Bulletin 1, 1–18.


DeWoody, J. A. , and Avise, J. C. (2001). Genetic perspectives on the natural history of fish mating systems. The Journal of Heredity 92, 167–172.
CrossRef | CAS | PubMed |

DeWoody, J. A. , Fletcher, D. E. , Mackiewicz, S. D. , Wilkins, S. D. , and Avise, J. C. (2000a). The genetic mating system of spotted sunfish (Lepomis punctatus): mate numbers and the influence of male reproductive parasites. Molecular Ecology 9, 2119–2128.
CrossRef | CAS | PubMed |

DeWoody, J. A. , Fletcher, D. E. , Wilkins, S. D. , and Avise, J. C. (2000b). Parentage and nest guarding in the tessellated darter (Etheostoma olmstedi) assayed by microsatellite markers (Perciformes: Percidae). Copeia 3, 740–747.
CrossRef |

DeWoody, J. A. , Fletcher, D. E. , Wilkins, S. D. , Nelson, W. S. , and Avise, J. C. (1998). Molecular genetic dissection of spawning, parentage, and reproductive tactics in a population of redbreast sunfish, Lepomis auritus. Evolution 52, 1802–1810.
CrossRef | CAS |

DeWoody, J. A. , Fletcher, D. E. , Wilkins, S. D. , Nelson, W. S. , and Avise, J. C. (2000c). Genetic monogamy and biparental care in externally fertilizing fish, the largemouth bass (Micropterus salmoides). Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 2431–2437.
CrossRef | CAS |

Ewens, W. J. (1982). On the concept of the effective population size. Theoretical Population Biology 21, 373–378.
CrossRef |

Fessehaye, Y. , El-Bialy, Z. , Rezk, M. , Crooijmans, R. , Bovenhuis, H. , and Komen, H. (2006). Mating systems and male reproductive success in Nile tilapia (Oreochromis niloticus) in breeding hapas: a microsatellite analysis. Aquaculture 256, 148–158.
CrossRef |

Ford, M. J. (2002). Selection in captivity during supportive breeding may reduce fitness in the wild. Conservation Biology 16, 815–825.
CrossRef |

Frankham R., Ballou J. D., and Briscoe D. A. (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambridge.)

Goudet, J. (1995). FSTAT (vers. 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.


Hill, W. G. (1981). Estimation of effective population size from data on linkage disequilibrium. Genetic Research Cambridge 38, 209–216.


Ingram, B. A. , De Silva, S. S. , and Gooley, G. J. (2005). The Australian Murray cod – a new candidate for intensive production systems. World Aquaculture 36, 37–43 and 69.


Jones, A. G. , Östlund-Nilsson, S. , and Avise, J. C. (1998). A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution 52, 848–858.
CrossRef |

Kvarnemo, C. , Moore, G. I. , Jones, A. G. , Nelson, W. S. , and Avise, J. C. (2000). Monogamous pair bonds and mate switching in the Western Australian seahorse Hippocampus subelongatus. Journal of Evolutionary Biology 13, 882–888.
CrossRef |

Lande R., and Barrowclough G. F. (1987). Effective population size, genetic variation, and their use in population management. In ‘Viable Populations for Conservation’. (Ed. M. E. Soulé.) pp. 87–123. (Cambridge University Press: Cambridge.)

Larsen, P. F. , Nielsen, E. E. , Williams, T. D. , Hemmer-Hansen, J. , Chipman, J. K. , Kruhøffer, M. , Grønkjær, P. , George, S. G. , Dyrskjøt, L. , and Loeschcke, V. (2007). Adaptive differences in gene expression in European flounder (Platichthys flesus). Molecular Ecology 16, 4674–4683.
CrossRef | CAS | PubMed |

Lemos, A. , Freitas, A. A. , Fernandes, A. T. , Gonçalves, R. , Jesus, J. , Andrade, C. , and Brehm, A. (2006). Microsatellite variability in natural populations of the blackspot seabream Pagellus bogaraveo (Brünnick, 1768): a database to access parentage assignment in aquaculture. Aquaculture and Research 37, 1028–1033.
CrossRef |

Loughnan, S. R. , Baranski, M. D. , Robinson, N. A. , Jones, P. L. , and Burridge, C. P. (2004). Microsatellite loci for studies of wild and hatchery Australian Murray cod Maccullochella peelii peelii (Percichthyidae). Molecular Ecology Notes 4, 382–384.
CrossRef | CAS |

Lynch, M. , and O’Hely, M. (2001). Captive breeding and the genetic fitness of natural populations. Conservation Genetics 2, 363–378.
CrossRef |

Marshall, T. C. , Slate, J. , Kruuk, L. E. B. , and Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7, 639–655.
CrossRef | CAS | PubMed |

Miller L. M., and Kapuscinski A. R. (2003). Genetic guidelines for hatchery supplementation programs. In ‘Population Genetics Principles and Applications for Fisheries Scientists’. (Ed. E. M. Hallerman.) pp. 329–355. (American Fisheries Society: Bethesda, MD.)

Newman, D. M. , Jones, P. L. , and Ingram, B. A. (2007). Temporal dynamics of oocyte development, plasma sex steroids and somatic energy reserves during seasonal ovarian maturation in captive Murray cod Maccullochella peelii peelii. Comparative Biochemistry and Physiology Part A 148, 876–887.
CrossRef |

Peel D., Ovenden J. R., and Peel S. L. (2004). NeEstimator: software for estimating effective population size (version 1.3). Queensland Government, Department of Primary Industries and Fisheries, Brisbane.

Pudovkin, A. I. , Zaykin, D. V. , and Hedgecock, D. (1996). On the potential for estimating the effective number of breeders from heterozygote excess in progeny. Genetics 144, 383–387.
CAS | PubMed |

Raymond, M. , and Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.


Rice, W. F. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
CrossRef |

Rico, C. , Kuhnlein, U. , and Fitzgerald, G. J. (1992). Male reproductive tactics in the threespine stickleback – an evaluation by DNA fingerprinting. Molecular Ecology 1, 79–87.
CrossRef |

Rourke M. L. (2007). Population genetic structure of Murray cod (Maccullochella peelii peelii) and impacts of stocking in the Murray–Darling Basin. Ph.D. Thesis, Monash University, Melbourne.

Rourke, M. , Nheu, J. , Mountford, H. , Lade, J. , and Ingram, B. , et al. (2007). Isolation and characterization of 102 new microsatellite loci in Murray cod, Maccullochella peelii peelii (Percichthyidae), and assessment of cross-amplification in 13 Australian native and six introduced freshwater species. Molecular Ecology Notes 7, 1258–1264.
CrossRef | CAS |

Rowe, G. , and Beebee, T. J. C. (2004). Reconciling genetic and demographic estimators of effective population size in the anuran amphibian Bufo calamita. Conservation Genetics 5, 287–298.
CrossRef | CAS |

Rowe, S. , Hutchings, J. A. , Skjæraasen, J. E. , and Bezanson, L. (2008). Morphological and behavioural correlates of reproductive success in Atlantic cod Gadus morhua. Marine Ecology Progress Series 354, 257–265.
CrossRef |

Rowland, S. J. (1983). Spawning of the Australian freshwater fish Murray cod, Maccullochella peeli (Mitchell), in earthen ponds. Journal of Fish Biology 23, 525–534.
CrossRef |

Rowland, S. J. (1988). Hormone-induced spawning of the Australian freshwater fish Murray cod (Maccullochella peeli (Mitchell)) (Percichthyidae). Aquaculture 70, 371–389.
CrossRef | CAS |

Rowland, S. J. (1989). Aspects of the history and fishery of the Murray Cod, Maccullochella peeli (Mitchell) (Percichthyidae). Proceedings of the Linnean Society of New South Wales 111, 201–213.


Rowland, S. J. (1998). Aspects of the reproductive biology of Murray cod, Maccullochella peelii peelii. Proceedings of the Linnean Society of New South Wales 120, 147–162.


Saccheri, K. , Mikko, K. , Kankare, M. , Vikman, P. , Fortelius, W. , and Hanski, I. (1998). Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494.
CrossRef | CAS |

Stockwell, C. A. , Mulvey, M. , and Vinyard, G. L. (1996). Translocations and the preservation of allelic diversity. Conservation Biology 10, 1133–1141.
CrossRef |

Takahashi, D. , and Ohara, K. (2006). Parentage analyses of freshwater goby Rhinogobius sp. OR using microsatellite DNA markers and egg developmental stages of eggs in the nest. Ichthylogcal Research 53, 87–92.
CrossRef |

Taylor A. C. (2003). Assessing the consequences of inbreeding for population fitness: past challenges and future prospects. In ‘Reproductive Science and Integrated Conservation’. (Eds W. V. Holt, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 67–81. (Cambridge University Press: Cambridge.)

Theodorou, K. , and Couvet, D. (2004). Introduction of captive breeders to the wild: Harmful or beneficial? Conservation Genetics 5, 1–12.
CrossRef |

Vrijenhoek, R. C. (1998). Conservation genetics of freshwater fish. Journal of Fish Biology 53(Suppl. A), 394–412.
CrossRef |

Wang, J. , and Ryman, N. (2001). Genetic effects of multiple generations of supportive breeding. Conservation Biology 15, 1619–1631.
CrossRef |

Welcomme, R. L. , and Bartley, D. M. (1998). Current approaches to the enhancement of fisheries. Fisheries Management and Ecology 5, 351–382.
CrossRef |

Wright, S. (1931). Evolution in mendelian populations. Genetics 16, 97–159.
CAS | PubMed |



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