ADAPTIVE DIVERGENCE AND THE BALANCE BETWEEN SELECTION AND GENE FLOW: LAKE AND STREAM STICKLEBACK IN THE MISTY SYSTEM

Abstract We investigated the interplay between natural selection and gene flow in the adaptive divergence of threespine stickleback (Gasterosteus aculeatus) that reside parapatrically in lakes and streams. Within the Misty Lake system (Vancouver Island, British Columbia), stickleback from the inlet stream (flowing into the lake) have fewer gill rakers and deeper bodies than stickleback from the lake—differences thought to facilitate foraging (benthic macroinvertebrates in the stream vs. zooplankton in the open water of the lake). Common-garden experiments demonstrated that these differences have a genetic basis. Reciprocal transplant enclosure experiments showed that lake and inlet stickleback grow best in their home environments (although differences were subtle and often not significant). Release-recapture experiments in the inlet showed that lake fish are less well-suited than inlet fish for life in the stream (higher mortality or emigration in lake fish). Morphological divergence in the wild and under common rearing was greater between the lake and the inlet than between the lake and the outlet. Genetic divergence (mitochondrial DNA and microsatellites) was greatest between the lake and the upper inlet (1.8 km upstream from the lake), intermediate between the lake and the lower inlet (0.9 km upstream), and least between the lake and the outlet stream (1.2 km downstream). Relative levels of gene flow estimated from genetic data showed the inverse pattern. The negative association between morphological divergence and gene flow is consistent with the expectation that gene flow can constrain adaptation. Estimated absolute levels of gene flow also implied a constraint on adaptation in the outlet but not the inlet. Our results suggest that natural selection promotes the adaptive divergence of lake and stream stickleback, but that the magnitude of divergence can be constrained by gene flow.

[1]  R. Chakraborty,et al.  Heterozygote deficiency, population substructure and their implications in DNA fingerprinting , 2004, Human Genetics.

[2]  S. J. Arnold,et al.  The adaptive landscape as a conceptual bridge between micro- and macroevolution , 2004, Genetica.

[3]  H. Rundle.  A TEST OF ECOLOGICALLY DEPENDENT POSTMATING ISOLATION BETWEEN SYMPATRIC STICKLEBACKS , 2002, Evolution; international journal of organic evolution.

[4]  K. M. Wegner,et al.  Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity , 2001, Molecular ecology.

[5]  A. Hendry,et al.  POPULATION MIXING AND THE ADAPTIVE DIVERGENCE OF QUANTITATIVE TRAITS IN DISCRETE POPULATIONS: A THEORETICAL FRAMEWORK FOR EMPIRICAL TESTS , 2001, Evolution; international journal of organic evolution.

[6]  J. M. Hoekstra,et al.  The Strength of Phenotypic Selection in Natural Populations , 2001, The American Naturalist.

[7]  H. Rundle,et al.  A GENETIC INTERPRETATION OF ECOLOGICALLY DEPENDENT ISOLATION , 2001, Evolution; international journal of organic evolution.

[8]  S. Gavrilets.  Waiting time to parapatric speciation , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  E. Taylor,et al.  Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  T. Quinn,et al.  Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. , 2000, Science.

[11]  G. M. Taylor.  Maximum force production: why are crabs so strong? , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[13]  G Luikart,et al.  New methods employing multilocus genotypes to select or exclude populations as origins of individuals. , 1999, Genetics.

[14]  D. Schluter,et al.  ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT‐DEPENDENT HYBRID FITNESS , 1999, Evolution; international journal of organic evolution.

[15]  J. Felsenstein,et al.  Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. , 1999, Genetics.

[16]  M. Whitlock,et al.  Indirect measures of gene flow and migration: FST≠1/(4Nm+1) , 1999, Heredity.

[17]  A. Storfer,et al.  Gene flow and endangered species translocations: a topic revisited , 1999 .

[18]  M. Feldman,et al.  Mutation and migration in models of microsatellite evolution , 1999 .

[19]  D. Cooper,et al.  Microsatellite markers for the Phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula) , 1998, Molecular ecology.

[20]  Stephen P Ellner,et al.  A SPATIALLY EXPLICIT STOCHASTIC MODEL DEMONSTRATES THE FEASIBILITY OF WRIGHT'S SHIFTING BALANCE THEORY , 1998, Evolution; international journal of organic evolution.

[21]  L. Bernatchez,et al.  Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  E. Taylor,et al.  PARALLEL EVOLUTION OF LAKE‐STREAM PAIRS OF THREESPINE STICKLEBACKS (GASTEROSTEUS) INFERRED FROM MITOCHONDRIAL DNA VARIATION , 1997, Evolution; international journal of organic evolution.

[23]  M. Kirkpatrick,et al.  Evolution of a Species' Range , 1997, The American Naturalist.

[24]  E. Taylor,et al.  Postglacial genetic differentiation of reproductive ecotypes of kokanee Oncorhynchus nerka in Okanagan Lake, British Columbia , 1997, Molecular ecology.

[25]  Mark Kirkpatrick,et al.  GENETIC MODELS OF ADAPTATION AND GENE FLOW IN PERIPHERAL POPULATIONS , 1997, Evolution; international journal of organic evolution.

[26]  Dolph Schluter,et al.  Ecological Speciation in Postglacial Fishes , 1996 .

[27]  D. Levin,et al.  Origins of endemic stickleback from the Queen Charlotte Islands: mitochondrial and morphological evidence , 1996 .

[28]  S. Palumbi,et al.  Nucleic acids II: the polymerase chain reaction , 1996 .

[29]  J. Goudet.  FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics , 1995 .

[30]  Jeffrey V. Baumgartner.  Phenotypic, genetic, and environmental integration of morphology in a stream population of the threespine stickleback, Gasterosteus aculeatus , 1995 .

[31]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[32]  D. Futuyma,et al.  Hybrid zones and the evolutionary process , 1995 .

[33]  Dolph Schluter,et al.  Adaptive Radiation in Sticklebacks: Trade‐Offs in Feeding Performance and Growth , 1995 .

[34]  A. Meyer,et al.  GLOBAL SURVEY OF MITOCHONDRIAL DNA SEQUENCES IN THE THREESPINE STICKLEBACK: EVIDENCE FOR RECENT MIGRATIONS , 1994, Evolution; international journal of organic evolution.

[35]  W. Rice,et al.  LABORATORY EXPERIMENTS ON SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS? , 1993, Evolution; international journal of organic evolution.

[36]  U. Kuhnlein,et al.  Characterization of hypervariable microsatellite loci in the threespine stickleback Gasterosteus aculeatus , 1993, Molecular ecology.

[37]  T. Reimchen,et al.  MITOCHONDRIAL DNA IN GASTEROSTEUS AND PLEISTOCENE GLACIAL REFUGIUM ON THE QUEEN CHARLOTTE ISLANDS, BRITISH COLUMBIA , 1993, Evolution; international journal of organic evolution.

[38]  J. Mcphail,et al.  Parapatric lake and stream sticklebacks on northern Vancouver Island: disjunct distribution or parallel evolution? , 1993 .

[39]  D. Schluter,et al.  Ecological Character Displacement and Speciation in Sticklebacks , 1992, The American Naturalist.

[40]  M. Whitlock.  TEMPORAL FLUCTUATIONS IN DEMOGRAPHIC PARAMETERS AND THE GENETIC VARIANCE AMONG POPULATIONS , 1992, Evolution; international journal of organic evolution.

[41]  E. Bermingham,et al.  REAP: an integrated environment for the manipulation and phylogenic analysis of restriction data. , 1992, The Journal of heredity.

[42]  M. Slatkin,et al.  A COMPARISON OF THREE INDIRECT METHODS FOR ESTIMATING AVERAGE LEVELS OF GENE FLOW , 1989, Evolution; international journal of organic evolution.

[43]  D. Roff,et al.  The statistical analysis of mitochondrial DNA polymorphisms: chi 2 and the problem of small samples. , 1989, Molecular biology and evolution.

[44]  J. M. Scott,et al.  Translocation as a Species Conservation Tool: Status and Strategy , 1989, Science.

[45]  L. Holtby,et al.  Differences in Morphology and Behavior between Juvenile Coho Salmon (Oncorhynchus kisutch) Rearing in a Lake and in its Tributary Stream , 1989 .

[46]  I. Walker,et al.  Early postglacial chironomid succession in southwestern British Columbia, Canada, and its paleoenvironmental significance , 1989 .

[47]  M Slatkin,et al.  Gene flow and the geographic structure of natural populations. , 1987, Science.

[48]  J. Endler.  Natural selection in the wild , 1987 .

[49]  J. Mcphail,et al.  Adaptive Divergence of Trophic Phenotype among Freshwater Populations of the Threespine Stickleback (Gasterosteus aculeatus) , 1986 .

[50]  E. Taylor,et al.  Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus , 1986 .

[51]  T. Reimchen,et al.  Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands , 1985 .

[52]  M. Slatkin.  RARE ALLELES AS INDICATORS OF GENE FLOW , 1985, Evolution; international journal of organic evolution.

[53]  P. Bentzen,et al.  Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair , 1984 .

[54]  M. Turelli.  Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle. , 1984, Theoretical population biology.

[55]  J. Anderson,et al.  Geographic Variation in the Gillrakers and Diet of European Threespine Sticklebacks, Gasterosteus aculeatus , 1984 .

[56]  B S Weir,et al.  Estimation of the coancestry coefficient: basis for a short-term genetic distance. , 1983, Genetics.

[57]  N. Takahata.  Gene identity and genetic differentiation of populations in the finite island model. , 1983, Genetics.

[58]  E. Stinson.  Threespine sticklebacks (Gasterosteus aculeatus) in Drizzle Lake and its inlet, Queen Charlotte Islands: ecological and behavioural relationships and their relevance to reproductive isolation , 1983 .

[59]  M. Bell.  DIFFERENTIATION OF ADJACENT STREAM POPULATIONS OF THREESPINE STICKLEBACKS , 1982, Evolution; international journal of organic evolution.

[60]  M. A. Bell,et al.  Clinal Variation of Lateral Plates in Threespine Stickleback Fish , 1981, The American Naturalist.

[61]  J. Endler.  Geographic variation, speciation, and clines. , 1977, Monographs in population biology.

[62]  J. Felsenstein.  The theoretical population genetics of variable selection and migration. , 1976, Annual review of genetics.

[63]  M. Slatkin.  Gene flow and selection in a cline. , 1973, Genetics.

[64]  G. Moodie.  Morphology, life history, and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada , 1972 .

[65]  G E E Moodie,et al.  Predation, natural selection and adaptation in an unusual threespine stickleback , 1972, Heredity.

[66]  D. Hagen,et al.  GEOGRAPHIC VARIATION AND ENVIRONMENTAL SELECTION IN GASTEROSTEUS ACULEATUS L. IN THE PACIFIC NORTHWEST, AMERICA , 1972, Evolution; international journal of organic evolution.

[67]  H. G. Baker,et al.  Differentiation of populations. , 1970, Science.