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Mating system and individual reproductive success of sympatric anadromous and resident brook charr, Salvelinus fontinalis, under natural conditions

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Abstract

Salmonids are known for the occurrence in sympatry of two life-history forms, one that undergoes migration to sea before returning to freshwater to reproduce (anadromous) and one that inhabits freshwater without a migration phase (resident). Whereas one breeding population is often suggested by population genetic studies, mating patterns have rarely been directly assessed, especially when both sexes are found within each life-history form. By using highly polymorphic microsatellite loci and parentage analysis in a natural population of sympatric anadromous and resident brook charr (Salvelinus fontinalis), we found that gene flow occurred between the two forms and was mediated by resident males mating with both resident and anadromous females. Determinants of reproductive success, estimated by the number of surviving juveniles (ages 1 and 2 years), differed between the sexes. No strong evidence of the influence of size on individual reproductive success was found for males, whereas larger females (and hence most likely to be anadromous) were more successful. The higher individual reproductive success of anadromous fish compared to residents was mainly explained by this higher reproductive success of anadromous females. We suggest that resident males adopt a “sneaking” reproductive tactic as a way of increasing their reproductive success by mating with females of all sizes in all habitats. The persistence of the resident tactic among females may be linked to their advantage in accessing spatially constrained spawning areas in small tributary streams unavailable to larger females.

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References

  • Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating system and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45

    Article  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2000) GENETIX 4.02, Logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614

    Article  Google Scholar 

  • Blanchfield PJ, Ridgway MS, Wilson CC (2003) Breeding success of male brook trout (Salvelinus fontinalis) in the wild. Mol Ecol 12:2417–2428

    Article  PubMed  Google Scholar 

  • Blomqvist D, Andersson M, Kupper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Szekely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature (Lond) 419:613–615

    Article  CAS  Google Scholar 

  • Bohlin T, Dellefors C, Faremo U (1994) Probability of first sexual maturation of male parr in wild sea-run brown trout (Salmo trutta) depends on condition factor 1 yr in advance. Can J Fish Aquat Sci 51:1920–1926

    Google Scholar 

  • Boula D, Castric V, Bernatchez L, Audet C (2002) Physiological, endocrine, and genetic bases of anadromy in the brook charr, Salvelinus fontinalis, of the Laval River (Quebec, Canada). Environ Biol Fish 64:229–242

    Article  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    Article  PubMed  CAS  Google Scholar 

  • Castric V, Bernatchez L (2003) The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163:983–996

    PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Bancroft DR, Robertson A, Smith J, Clutton-Brock TH, Pemberton JM (1999) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol Ecol 8:1199–1209

    Article  PubMed  CAS  Google Scholar 

  • Conrad KF, Johnston PV, Crossman C, Kempenaers B, Robertson RJ, Wheelwright NT, Boag T (2001) High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor). Mol Ecol 10:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  PubMed  CAS  Google Scholar 

  • DeHaan PW, Ardren WR (2005) Characterization of 20 highly variable tetranucleotide microsatellite for bull trout (Salvelinus confluentus) and cross amplification in other Salvelinus species. Mol Ecol Notes 5:582–585

    Article  CAS  Google Scholar 

  • DeWoody JA, Avise JC (2001) Genetic perspectives on the natural history of fish mating systems. J Hered 92:167–172

    Article  PubMed  CAS  Google Scholar 

  • Dickerson BR, Willson MF, Bentzel P, Quinn TP (2004) Size-assortative mating in salmonids: negative evidence for pink salmon in natural conditions. Anim Behav 68:381–385

    Article  Google Scholar 

  • Dickerson BR, Brinck KW, Willson MF, Bentzen P, Quinn TP (2005) Relative importance of salmon body size and arrival time at breeding grounds to reproductive success. Ecology 86:347–352

    Article  Google Scholar 

  • Docker MF, Heath DD (2003) Genetic comparison between sympatric anadromous steelhead and freshwater resident rainbow trout in British Columbia, Canada. Conserv Genet 4:227–231

    Article  CAS  Google Scholar 

  • Doucett RR, Power M, Power G, Caron F, Reist JD (1999) Evidence for anadromy in a southern relict population of Arctic charr from North America. J Fish Biol 55:84–93

    Article  Google Scholar 

  • Duchesne P, Castric T, Bernatchez L (2005) PASOS (parental allocation of singles in open systems): a computer program for individual parental allocation with missing parents. Mol Ecol Notes 5:701–704

    Article  CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2004) Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58:2332–2342

    PubMed  CAS  Google Scholar 

  • Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fish 6:379–416

    Article  Google Scholar 

  • Fleming IA (1998) Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can J Fish Aquat Sci 55:59–76

    Article  Google Scholar 

  • Fleming IA, Gross MR (1994) Breeding competition in a Pacific salmon (Coho, Oncorhynchus kisutch)—measures of natural and sexual selection. Evolution 48:637–657

    Article  Google Scholar 

  • Fleming IA, Lamberg A, Jonsson B (1997) Effects of early experience on the reproductive performance of Atlantic salmon. Behav Ecol 8:470–480

    Article  Google Scholar 

  • Foote CJ (1990) An experimental comparison of male and female spawning territoriality in a Pacific salmon. Behaviour 115:283–314

    Google Scholar 

  • Foote CJ, Wood CC, Withler RE (1989) Biochemical genetic comparison of sockeye salmon and kokanee, the anadromous and nonanadromous forms of Oncorhynchus nerka. Can J Fish Aquat Sci 46:149–158

    Google Scholar 

  • Garant D, Dodson JJ, Bernatchez L (2001) A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). J Hered 92:137–145

    Article  PubMed  CAS  Google Scholar 

  • Garant D, Dodson JJ, Bernatchez L (2003) Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic Salmon (Salmo salar L.). Evolution 57:1133–1141

    PubMed  Google Scholar 

  • Garant D, Dodson JJ, Bernatchez L (2005) Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar). Behav Ecol Sociobiol 57:240–244

    Article  Google Scholar 

  • Garcia-Vazquez E, Moran P, Martinez JL, Perez J, de Gaudemar B, Beall E (2001) Alternative mating strategies in Atlantic salmon and brown trout. J Hered 92:146–149

    Article  PubMed  CAS  Google Scholar 

  • Gross MR (1987) Evolution of diadromy in fishes. Am Fish Soc Symp 1:14–25

    Google Scholar 

  • Hazel W, Smock R, Johnsson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc Biol Sci 242:181–188

    Article  PubMed  CAS  Google Scholar 

  • Hendry AP, Day T, Taylor EB (2001) Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. Am Nat 157:387–407

    Article  PubMed  CAS  Google Scholar 

  • Hindar K, Jonsson K, Rymon N, Stahl S (1991) Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L. Heredity 66:83–91

    Google Scholar 

  • Holtby LB, Healey MC (1986) Selection for adult size in female coho salmon (Oncorhynchus kisutch). Can J Fish Aquat Sci 43:1946–1959

    Article  Google Scholar 

  • Hughes CR (1998) Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology 79:383–399

    Article  Google Scholar 

  • Hutchings JA, Jones MEB (1998) Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar. Can J Fish Aquat Sci 55:22–47

    Article  Google Scholar 

  • Hutchings JA, Myers RA (1988) Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar. Oecologia (Berl) 75:169–174

    Article  Google Scholar 

  • Jones MW, Hutchings J (2002) Individual variation in Atlantic salmon fertilization success: implications for effective population size. Ecol Appl 12:184–193

    Article  Google Scholar 

  • Jones MW, Danzman RG, Clay D (1997) Genetic relationship among populations of wild resident, and wild and hatchery anadromous brook charr. J Fish Biol 51:29–40

    Article  PubMed  Google Scholar 

  • Jones AG, Östlund-Nilsson S, Avise JC (1998) A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution 52:848–858

    Article  Google Scholar 

  • Jonsson B (1985) Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Trans Am Fish Soc 114:182–194

    Article  Google Scholar 

  • Jonsson B, Hindar K (1982) Reproductive strategy of dwarf and normal Arctic charr (Salvelinus alpinus) from Vangsvatnet Lake, Western Norway. Can J Fish Aquat Sci 39:1404–1413

    Google Scholar 

  • Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365

    Article  Google Scholar 

  • Kempenaers B, Everding S, Bishop C, Boag P, Robertson RJ (2001) Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 49:251–259

    Article  Google Scholar 

  • Kristoffersen K, Halvorsen M, Jorgensen L (1994) Influence of parr growth, lake morphology and freshwater parasites on the degree of anadromy in different populations of Arctic charr (Salvelinus alpinus) in northern Norway. Can J Fish Aquat Sci 51:1229–1246

    Article  Google Scholar 

  • Lenormand S (2003) Évolution de l’anadromie et stratégie de reproduction chez l’omble de fontaine, (Salvelinus fontinalis). PhD thesis. Biologie Université Laval, Québec, 122 pp

  • Lenormand S, Dodson JJ, Ménard A (2004) Seasonal and ontogenetic patterns in the migration of anadromous brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 61:54–67

    Article  Google Scholar 

  • Lukasik P, Radwan J, Tomkins JL (2006) Structural complexity of the environment affects the survival of alternative male reproductive tactics. Evolution 60:399–403

    Article  PubMed  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Morinville GR, Rasmussen JB (2003) Early juvenile bioenergetic differences between anadromous and resident brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60:401–410

    Article  Google Scholar 

  • Morita K, Takashima Y (1998) Effect of female size on fecundity and egg size in white-spotted charr: comparison between sea-run and resident forms. J Fish Biol 53:1140–1142

    Article  Google Scholar 

  • Morita K, Yamamoto S, Hoshino N (2000) Extreme life history change of white-spotted charr (Salvelinus leucomaenis) after damming. Can J Fish Aquat Sci 57:1300–1306

    Article  Google Scholar 

  • Narum SR, Control C, Talbot A, Powee MS (2004) Genetic divergence of sympatric resident and anadromous forms of Oncorhynchus mykiss in the Walla Walla River, USA J Fish Biol 65:471–488

    Article  Google Scholar 

  • Neff BD (2001) Genetic paternity analysis and breeding success in bluegill sunfish (Lepomis macrochiros). J Hered 92:111–119

    Article  PubMed  CAS  Google Scholar 

  • Nordeng H (1983) Solution to the ‘Char Problem’ based on Arctic char (Salvelinus alpinus) in Norway. Can J Fish Aquat Sci 40:1372–1387

    Google Scholar 

  • Olsson IC, Greenberg LA (2004) Partial migration in a landlocked brown trout population. J Fish Biol 65:106–121

    Article  Google Scholar 

  • Pemberton JM, Slate J, Bancroft DR, Barrett A (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252

    PubMed  CAS  Google Scholar 

  • Perry GML, King T, Valcourt M, St-Cyr J, Bernatchez L (2005) Isolation and cross amplification of forty-three microsatellites for the brook charr (Salvelinus fontinalis). Mol Ecol Notes 5:346–351

    Article  CAS  Google Scholar 

  • Quinn TP, Foote CJ (1994) The effect of body size and sexual dimorphism on the reproductive behaviour of sockeye salmon, Oncorhynchus nerka. Anim Behav 48:751–761

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 11:68–72

    Article  Google Scholar 

  • Rikardsen AH, Svenning M-A, Klemetsen A (1997) The relationship between anadromy, sex ratio and parr growth of Arctic charr in a lake in north Norway. J Fish Biol 51:447–461

    Article  Google Scholar 

  • Roff DA (1996) The evolution of threshold traits in animals. Q Rev Biol 71:3–35

    Article  Google Scholar 

  • Rosenberger AE, Dunham JB (2005) Validation of abundance estimates from mark-recapture and removal techniques for rainbow trout captured by electrofishing in small streams. N Am J Fish Manag 25:1396–1410

    Article  Google Scholar 

  • Schreiber A, Diefenbach G (2005) Population genetics of the European trout (Salmo trutta L.) migration system in the river Rhine: recolonisation by sea trout. Ecol Freshw Fish 14:1–13

    Article  Google Scholar 

  • Scott MP, Williams SM (1993) Comparative reproductive success of communally breeding burying beetles as assessed by PCR with randomly amplified polymorphic DNA. Proc Natl Acad Sci USA 90:2242–2245

    Article  PubMed  CAS  Google Scholar 

  • Seamons TR, Bentzel P, Quinn TP (2004a) The effects of adult length and arrival date on individual reproductive success in wild steelhead trout (Oncorhyncus mykiss). Can J Fish Aquat Sci 61:193–204

    Article  Google Scholar 

  • Seamons TR, Bentzen P, Quinn TP (2004b) The mating system of steelhead, Oncorhynchus mykiss, inferred by molecular analysis of parents and progeny. Environ Biol Fish 69:333–344

    Article  Google Scholar 

  • Steen RP, Quinn TP (1999) Egg burial depth by sockeye salmon (Oncorhynchus nerka): implications for survival of embryos and natural selection on female body size. Can J Zool 77:836–841

    Article  Google Scholar 

  • Thériault V, Dodson JJ (2003) Body size and the adoption of a migratory tactic in brook charr. J Fish Biol 63:1144–1159

    Article  Google Scholar 

  • Thomaz D, Beall E, Burke T (1997) Alternative reproductive tactics in Atlantic salmon: factors affecting mature parr success. Proc R Soc Lond B Biol Sci 264:219–226

    Article  Google Scholar 

  • Tsiger VV, Skirin VI, Krupyanko NI, Kashkin KA, Semenchenko AY (1994) Life history forms of male masu salmon (Oncorhynchus masou) in South Primor’e, Russia. Can J Fish Aquat Sci 51:197–208

    Google Scholar 

  • Unwin MJ, Kinnison MT, Quinn TP (1999) Exceptions to semelparity: postmaturation survival, morphology, and energetics of male chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 56:1172–1181

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Westneat DF (1987) Extra-pair fertilizations in a predominantly monogamous bird: genetic evidence. Anim Behav 35:877–886

    Article  Google Scholar 

  • Wood CC, Foote CJ (1990) Genetic differences in the early development and growth of sympatric sockeye salmon and kokanee (Oncorhynchus nerka), and their hybrids. Can J Fish Aquat Sci 47:2250–2260

    Article  Google Scholar 

  • Wood CC, Foote CJ (1996) Evidence for sympatric genetic divergence of anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 50:1265–1279

    Article  Google Scholar 

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Acknowledgments

We acknowledge A. Boivin, S. Bordeleau, M. Foy-Guitard, S.-P. Gingras, Fannie Martin, François Martin, A. Ménard, G. Morinville, L. Papillon, L. V. St-Hilaire Gravel, and R. St-Laurent for the field assistance and laboratory work. The authors would like to thank P. Duchesne for the helpful advice and assistance in the use of the software PASOS and D. Garant for the helpful comments on a draft version of this manuscript. Funding of this project was provided to J.J.D. and L.B. by NSERC of Canada (Strategic Grant and Collaborative Special Projects), the Fondation de la Faune du Québec, the Government of Québec (FAPAQ), the Government of Canada (Economic development), and the financial partners of AquaSalmo R&D. This study is a contribution to the program of CIRSA (Centre interuniversitaire de recherche sur le saumon Atlantique) and Quebec-Ocean. V.T. was financially supported by funding from NSERC and FQRNT. The experiments conducted comply with the current Canadian laws.

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  1. Université Laval, Département de biologie, Cité Universitaire, Québec, G1K 7P4, PQ, Canada

    Véronique Thériault, Louis Bernatchez & Julian J. Dodson

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  1. Véronique Thériault
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  2. Louis Bernatchez
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  3. Julian J. Dodson
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Correspondence to Julian J. Dodson.

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Thériault, V., Bernatchez, L. & Dodson, J.J. Mating system and individual reproductive success of sympatric anadromous and resident brook charr, Salvelinus fontinalis, under natural conditions. Behav Ecol Sociobiol 62, 51–65 (2007). https://doi.org/10.1007/s00265-007-0437-8

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