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Fluctuating sex ratios, but no sex-biased dispersal, in a promiscuous fish

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Abstract

Dispersal in birds and mammals tends to be female-biased in monogamous species and male-biased in polygamous species. However results for other taxa, most notably fish, are equivocal. We employed molecular markers and physical tags to test the hypothesis that Atlantic salmon, a promiscuous species with intense male-male competition for access to females, displays male-biased dispersal. We found significant variation in sex ratios and in asymmetric gene flow between neighbouring salmon populations, but little or no evidence for sex-biased dispersal. We show that conditions favouring male dispersal will often be offset by those favouring female dispersal, and that spatial and temporal variation in sex ratios within a metapopulation may favour the dispersal of different sexes in source and sink habitats. Thus, our results reconcile previous discrepancies on salmonid dispersal and highlight the need to consider metapopulation dynamics and sex ratios in the study of natal dispersal of highly fecund species.

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References

  • Aars J, Ims RA (2000) Population dynamic and genetic consequences of spatial density-dependent dispersal in patchy populations. Am Nat 155:252–265

    Article  PubMed  Google Scholar 

  • Aparicio E, de Sostoa A (1999) Pattern of movements of adult Barbus haasi in a small Mediterranean stream. J Fish Biol 55:1086–1095

    Article  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    Article  PubMed  CAS  Google Scholar 

  • Bekkevold D, Hansen MM, Mensberg KD (2004) Genetic detection of sex-specific dispersal in historical and contemporary populations of anadromous brown trout Salmo trutta. Mol Ecol 13:1707–1712

    Article  PubMed  CAS  Google Scholar 

  • Birky CW, Fuerst P, Maruyama T (1989) Organelle diversity under migration, mutation and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparisons to nuclear genes. Genetics 121:613–627

    PubMed  Google Scholar 

  • Blundell GM, Ben-David M, Groves P, Bowyers RT, Geffen E (2002) Characteristics of sex-biased dispersal and gene flow in coastal river otters: implications for natural recolonization of extirpated populations. Mol col 11:289–303

    CAS  Google Scholar 

  • Buonaccorsi VP, McDowell JR, Graves JE (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 10:1179–1196

    Article  PubMed  CAS  Google Scholar 

  • Croft DP, Albanese B, Arrowsmith BJ, Botham M, Webster M, Krause J (2003) Sex-biased movement in the guppy (Poecilia reticulata). Oecologia 137:62–68

    Article  PubMed  Google Scholar 

  • Cadet C, Ferrière R, Metz JAJ, van Baalen M (2003) The evolution of dispersal under demographic stochasticity. Am Nat 162:427–441

    Article  PubMed  Google Scholar 

  • Caudill CC (2003) Measuring dispersal in a metapopulation using stable isotope enrichment: high rates of ex-biased dispersal between patches in a mayfly metapopulation. Oikos 101:624–630

    Article  Google Scholar 

  • Clobert J, Nichols JD, Danchin E, Dhondt A (2001) Dispersal. Oxford University Press, Oxford, UK

    Google Scholar 

  • Cohen D, Levin SA (1991) Dispersal in patchy environments: the effects of temporal and spatial structure. Theor Popul Biol 39:63–69

    Article  Google Scholar 

  • Consuegra S, García de Leániz C, Serdio A, González Morales M, Straus LG, Knox D, Verspoor E (2002) Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium. Mol Ecol 11:2037–2048

    Article  PubMed  CAS  Google Scholar 

  • Consuegra S, Verspoor E, Knox D, García de Leániz C (2005a) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Cons Genetics 6:823–842

    Article  CAS  Google Scholar 

  • Consuegra S, García de Leániz C, Serdio A, Verspoor E (2005b) Selective exploitation of early running fish may induce genetic and phenotypic changes in Atlantic salmon. J Fish Biol 67(␣Suppl. A):130–146

    Google Scholar 

  • Dobson FS (1982) Competition for mates and predominant juvenile dispersal in mammals. Anim Behav 30:1183–1192

    Article  Google Scholar 

  • Dobson FS, Jones WT (1985) Multiple causes of dispersal. Am Nat 126:855–858

    Article  Google Scholar 

  • Escorza-Treviño S, Dizon AE (2000) Phylogeography, intraspecific structure and sex-biased dispersal of Dall’s porpoise, Phocoenoides dalli, revealed by mitochondrial and microsatellite DNA analyses. Mol Ecol 9:1049–1060

    Article  PubMed  Google Scholar 

  • Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc R Soc Lond B264:127–132

    Article  Google Scholar 

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

    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, Reynolds JD (2004) Salmonid breeding systems. In: Hendry AP, Stearns SC (eds) Evolution illuminated. Salmon and their relatives. New York: Oxford University Press, pp 264–294

    Google Scholar 

  • Fraser DJ, Lippé C, Bernatchez L. (2004) Consequences of unequal population size, asymmetric gene flow and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis) Mol Ecol 13:67–80

    Article  PubMed  CAS  Google Scholar 

  • Friedenberg NA (2003) Experimental evolution of dispersal in spatiotemporally variable microcosms. Ecol Lett 6:953–959

    Article  Google Scholar 

  • Garant D, Fontaine P-M, Good SP, Dodson JJ, Bernatchez L (2002) The influence of male parental identity on growth and survival of offspring in Atlantic salmon (Salmo salar). Evol Ecol Res 4:537–549

    Google Scholar 

  • Garant D, Kruuk LEB, Wilkin TA, McCleery RH, Sheldon BC (2005) Evolution driven by differential dispersal within a wild bird population. Nature 433:60–64

    Article  PubMed  CAS  Google Scholar 

  • Gilliam JF, Fraser DF (2001) Movement in corridors: enhancement by predation threat, disturbance, and habitat structure. Ecology 82:258–273

    Article  Google Scholar 

  • Glebe BD, Saunders RL (1986) Genetic factors in sexual maturity of cultured Atlantic salmon (Salmo salar) parr and adults reared in sea cages. Can Sp Pub Fish Aquat Sci 89:24–29

    Google Scholar 

  • Goudet J, Perrin N, Waser P. (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114

    Article  PubMed  CAS  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite DNA markers. Fish Fisher 2:93–112

    Article  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, New York

    Google Scholar 

  • Hard JJ, Heard WR (1999) Analysis of straying variation in Alaskan hatchery chinook salmon (Oncorhynchus tshawytscha) following transplantation. Can J Fish Aquat Sci 56:578–589

    Article  Google Scholar 

  • Hendry AP (2004) Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol Ecol Res 6:1219–1236

    Google Scholar 

  • Hendry AP, Castric V, Kinnison MT, Quinn TP (2004) The evolution of philopatry and dispersal. In: Hendry AP, Stearns SC (eds) Evolution illuminated. Salmon and their relatives. Oxford University Press, New York, pp. 52–91

    Google Scholar 

  • Hoarau G, Piquet AM T, van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190

    Article  CAS  Google Scholar 

  • Holt RD, McPeek MA (1996) Chaotic population dynamics favors the evolution of dispersal. Am Nat 148:709–718

    Article  Google Scholar 

  • Holtby LB, Healey MC (1990) Sex-specific life history tactics and risk-taking in coho salmon. Ecology 71:678–690

    Article  Google Scholar 

  • Huse G. (1998) Sex-specific life history strategies in capelin (Mallotus villosus). Can J Fish Aquat Sci 55:631–638

    Article  Google Scholar 

  • Hutchings JA, Gerber L. (2002) Sex-biased dispersal in a salmonid fish. Proc R Soc Lond B269:2487–2493

    Google Scholar 

  • Jones MW, Hutchings JA (2001) The influence of male parr body size and mate competition on fertilization success and effective population size in Atlantic salmon. Heredity 86:675–684

    Article  PubMed  CAS  Google Scholar 

  • Kawecki TJ, Holt RD (2002) Evolutionary consequences of asymmetric dispersal rates. Am Nat 160:333–347

    Article  PubMed  Google Scholar 

  • Knight ME, Van Oppen MJ H, Smith HL, Rico C, Hewitt GM, Turner GF (1999) Evidence for male-biased dispersal in Lake Malawi cichlids from microsatellites. Mol Ecol 8:1521–1527

    Article  PubMed  Google Scholar 

  • Koizumi I, Yamamoto S, Maekawa K. (2006) Female-biased migration of stream-dwelling Dolly Varden in the Shiisorapuchi River, Hokkaido, Japan. J Fish Biol 68:1513–1529

    Article  Google Scholar 

  • Le Galliard J-F, Ferrière R, Clobert J. (2003) Mother-offspring interactions affect natal dispersal in a lizard. Proc R Soc Lond B270:1163–1169

    Article  Google Scholar 

  • Leturque H, Rousset F. (2004) Intersexual competition as an explanation for sex-ratio and dispersal biases in polygynous species. Evolution 58:2398–2408

    Article  PubMed  Google Scholar 

  • Lundqvist H, McKinnell S, Fängstam H, Berglund I. (1994) The effect of time, size and sex on recapture rates and yield after river releases of Salmo salar smolts. Aquaculture 121:245–257

    Article  Google Scholar 

  • Massot M, Clobert J. (2000) Processes at the origin of similarities in dispersal behaviour among siblings. J Evol Biol 13:707–719

    Article  Google Scholar 

  • Mazluff JM, Balda RP. (1989) Causes and consequences of female biased dispersal in a flock-living bird, the pinyon jay. Ecology 70:316–328

    Article  Google Scholar 

  • Morbey Y. (2000) Protandry in Pacific salmon. Can J Fish Aquat Sci 57:1252–1257

    Article  Google Scholar 

  • Myers RA (1984) Demographic consequences of precocious maturation of Atlantic salmon (Salmo salar) Can J Fish Aquat Sci 41:1349–1353

    Article  Google Scholar 

  • Nagata M, Irvine JR (1997) Differential dispersal patterns of male and female masu salmon fry. J␣Fish Biol 51:601–606

    Article  Google Scholar 

  • Okuda N. (1999) Female mating strategy and male brood cannibalism in a sand-dwelling cardinalfish. Anim Behav 58:273–279

    Article  PubMed  Google Scholar 

  • Palo JU, Lesbarrères D, Schmeller DS, Primmer CR, Merilä J. (2004) Microsatellite marker data suggest sex-biased dispersal in the common frog Rana temporaria. Mol Ecol 13:2865–2869

    Article  PubMed  CAS  Google Scholar 

  • Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CA J, Martin AP (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140

    Article  PubMed  CAS  Google Scholar 

  • Paterson S, Piertney SB, Knox D, Gilbey J, Verspoor E. (2004) Characterization and PCR multiplexing of novel highly variable tetranucleotide Atlantic salmon (Salmo salar L.) microsatellites. Mol Ecol Notes 4:160–162

    Article  CAS  Google Scholar 

  • Perrin N, Mazalov V. (1999) Dispersal and inbreeding avoidance. Am Nat 154:282–292

    Article  PubMed  Google Scholar 

  • Perrin N, Mazalov V. (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127

    Article  PubMed  Google Scholar 

  • Poethke HJ, Hovestadt T. (2002) Evolution of density-and patch-size-dependent dispersal rates. Proc R Soc Lond B269:637–645

    Article  Google Scholar 

  • Prugnolle F, de Meeus T. (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165

    Article  PubMed  CAS  Google Scholar 

  • Ranta E, Lummaa V, Kaitala V, Merilä J. (2000) Spatial dynamics of adaptive sex ratios. Ecol Let 3:30–34

    Article  Google Scholar 

  • Russell ST, Kelley JL, Graves JA, Magurran AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106:520–526

    Article  Google Scholar 

  • Schleusner CJ, Maughan OE (1999) Mobility of largemouth bass in a desert lake in Arizona. Fish Res 44:175–178

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN ver 2.000: a sofware for populations genetics data analysis. Geneve: Genetics and Biometry Laboratory, University of Geneve

    Google Scholar 

  • Schradin C, Lamprecht J. (2000) Female-biased immigration and male peace-keeping in groups of the shell-dwelling cichlid fish Neolamprologus multifasciatus. Behav Ecol Sociobiol 48:236–242

    Article  Google Scholar 

  • Schrey AW, Heist EJ (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus ). Can J Fish Aquat Sci 60:670–675

    Article  CAS  Google Scholar 

  • Slatkin M. (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73

    Article  PubMed  Google Scholar 

  • Spidle AP, Quinn TP, Bentzen P. (1998) Sex-biased marine survival and growth in a population of coho salmon. J Fish Biol 52:907–915

    Article  Google Scholar 

  • Stiver KA, Dierkes P, Taborsky M, Balshine S. (2004) Dispersal patterns and status change in a co-operatively breeding cichlid Neolamprologus pulcher: evidence from microsatellite analyses and behavioural observations. J Fish Biol 65:981–105

    Article  Google Scholar 

  • Taggart JB, McLaren IS, Hay DW, Webb JH, Youngson AF (2001) Spawning success in Atlantic salmon (Salmo salar L.): a long-term DNA profiling-based study conducted in a natural stream. Mol Ecol 10:1047–1060

    Article  PubMed  CAS  Google Scholar 

  • Tamate T, Maekawa K (2004) Female-biased mortality rate and sexual size dimorphism of migratory masu salmon, Oncorhynchus masou. Ecol Freshw Fish 13:96–103

    Article  Google Scholar 

  • Taylor MI, Morley JI, Rico C, Balshine S. (2003) Evidence for genetic monogamy and female-biased dispersal in the biparental mouthbrooding cichlid Eretmodus cyanostictus from Lake Tanganyika. Mol Ecol 12:3173–3177

    Article  PubMed  Google Scholar 

  • Thedinga JF, Wertheimer AC, Heintz RA, Maselko JM, Rice SD (2000) Effects of stock, coded-wire tagging, and transplant on straying of pink salmon (Oncorhynchus gorbuscha) in southeastern Alaska. Can J Fish Aquat Sci 57:2076–2085

    Article  Google Scholar 

  • Unwin MJ, Quinn TP (1993) Homing and straying patterns of chinook salmon (Oncorhynchus tshawytscha) from a New Zealand hatchery: spatial distribution of strays and effects of release date. Can J Fish Aquat Sci 50:1168–1175

    Article  Google Scholar 

  • Wilson AJ, Hutchings JA, Ferguson MM (2004) Dispersal in a stream dwelling salmonid: inferences from tagging and microsatellite studies. Cons Genetics 5:25–37

    Article  CAS  Google Scholar 

  • Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy ICW (eds) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK, pp 48–92

    Google Scholar 

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Acknowledgements

We thank A. Serdio and the Cantabrian wildlife bailiffs for help with the collection of samples, and Pat Lee, Craig Primmer and four anonymous reviewers for helpful comments that greatly improved the manuscript. S. Consuegra was supported by the Fundacion Marcelino Botin.

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  1. Sofía Consuegra

    Present address: Department of Biological Sciences, University of Wales Swansea, Swansea, SA2 8PP, UK

Authors and Affiliations

  1. Department of Biological Sciences, University of Wales Swansea, Swansea, SA2 8PP, UK

    Carlos García de Leániz

  2. Gatty Marine Institute, University of St. Andrews, St. Andrews, Fife, KY16 8LB, Scotland, UK

    Sofía Consuegra

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  1. Sofía Consuegra
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Correspondence to Sofía Consuegra.

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Consuegra, S., García de Leániz, C. Fluctuating sex ratios, but no sex-biased dispersal, in a promiscuous fish. Evol Ecol 21, 229–245 (2007). https://doi.org/10.1007/s10682-006-9001-7

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