Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits

The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused...

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Published inMolecular ecology Vol. 19; no. 18; pp. 4061 - 4076
Main Authors ALDENHOVEN, JACLYN T., MILLER, MATTHEW A., CORNELI, PATRICE SHOWERS, SHAPIRO, MICHAEL D.
Format Journal Article
LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.09.2010
Subjects
Online AccessGet full text
ISSN0962-1083
1365-294X
1365-294X
DOI10.1111/j.1365-294X.2010.04801.x

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Abstract The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia—the Mississippi, Bering, and Atlantic refugia—not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.
AbstractList The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya-1 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia-the Mississippi, Bering, and Atlantic refugia-not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya-1 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia-the Mississippi, Bering, and Atlantic refugia-not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.
The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia—the Mississippi, Bering, and Atlantic refugia—not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.
The current geographical distribution of the ninespine stickleback ( Pungitius pungitius ) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia—the Mississippi, Bering, and Atlantic refugia—not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.
The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya-1 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia-the Mississippi, Bering, and Atlantic refugia-not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.
The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya-10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia--the Mississippi, Bering, and Atlantic refugia--not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia. [PUBLICATION ABSTRACT]
Author ALDENHOVEN, JACLYN T.
MILLER, MATTHEW A.
CORNELI, PATRICE SHOWERS
SHAPIRO, MICHAEL D.
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Bell MA, Orti G (1994) Pelvic reduction in threespine sticklebacks from Cook Inlet lakes: geographical distribution and intrapopulation variation. Copeia, 1994, 314-325.
Elias SA, Short SK, Nelson CH, Birks HH (1996) Life and times of the Bering land bridge. Nature, 382, 60-63.
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9, 299-306.
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704.
Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics, 144, 389-399.
Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN Version 2.0: A Software for Population Genetics Data Analysis. University of Geneva, Geneva.
Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233-257.
Takahashi H, Goto A (2001) Evolution of East Asian ninespine sticklebacks as shown by mitochondrial DNA control region sequences. Molecular Phylogenetics and Evolution, 21, 135-155.
Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Molecular Ecology, 7, 431-452.
Marchinko KB (2009) Predation's role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution, 63, 127-138.
Reynolds M, Weir BS, Cockerham CC (1983) Estimation for the coancestry coefficient: basis for a short term genetic distance. Genetics, 105, 767-779.
Reimchen TE (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Canadian Journal of Zoology, 58, 1232-1244.
Lu G, Basley DJ, Bernatchez L (2001) Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Molecular Ecology, 10, 965-985.
Shapiro MD, Bell MA, Kingsley DM (2006) Parallel genetic origins of pelvic reduction in vertebrates. Proceedings of the National Academy of Science, 103, 13753-13758.
Protas ME, Hersey C, Kochanek D et al. (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nature Genetics, 38, 107-111.
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457-462.
Lindsey CC (1981) Stocks are chameleons: plasticity in gill-rakers of coregonid fishes. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1497-1506.
Chan YF, Marks ME, Jones FC et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx 1 enhancer. Science, 327, 302-305.
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
Miller CT, Beleza S, Pollen AA et al. (2007) cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell, 131, 1179-1189.
Hansen MM, Mesberg K-L, Berg S (1999) Postglacial recolonization patterns and genetic relationships among whitefish (Coregonus sp.) populations in Denmark, inferred from mitochondrial DNA and microsatellite markers. Molecular Ecology, 8, 239-252.
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature, 405, 907-913.
Gross JB, Borowsky R, Tabin CJ (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genetics, 5, e1000326.
Gonda A, Herczeg G, Merila J (2009) Adaptive brain size divergence in nine-spined sticklebacks (Pungitius pungitius)? Journal of Evolutionary Biology, 22, 1721-1726.
Giles N (1983) The possible role of environmental calcium levels during the evolution of phenotypic diversity on Outer Hebridean populations of the three-spined stickleback, Gasterosteus aculeatus. Journal of Zoology, 4, 535-544.
Waser W, Sahoo TP, Herczeg G, Merilä J, Nikinmaa M (2010) Physiological differentiation among nine-spined stickleback populations: effects of copper exposure. Aquatic Toxicology, 98, 188-195.
Rempel LL, Smith DG (1998) Postglacial fish dispersal from the Mississippi refuge to the Mackenzie River basin. Canadian Journal of Fisheries and Aquatic Sciences, 55, 893-899.
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
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Karlstrom TNV (1964) Quaternary geology of the Kenai lowland and glacial history of the Cook Inlet region, Alaska. USGS Professional Paper, 443, 1-69.
Smith DG, Fisher TG (1993) Glacial Lake Agassiz: the northwestern outlet and paleoflood. Geology, 21, 9-12.
Ward JL, McLennan DA (2009) Historical and ecological correlates of body shape in the brook stickleback, Culaea inconstans. Biological Journal of the Linnean Society, 96, 769-783.
Bell MA, Orti G, Walker JA, Koenings JP (1993) Evolution of pelvic reduction in threespine stickleback fish: a test of competing hypotheses. Evolution, 47, 906-914.
Ho SYW, Larson G (2006) Molecular clocks: when times are a changin'. TRENDS in Genetics, 22, 79-83.
Craig BG (1965) Glacial Lake McConnell, and the superficial geology of parts of Slave River and Redstone River map areas, District of Mackenzie. Bulletin Geological Survey of Canada, 122, 33.
Walters V (1955) Fishes of western arctic America and eastern arctic Siberia. Bulletin of the American Museum of Natural History, 106, 255-368.
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185-1192.
Gross HP (1979) Geographic variation in European ninespine sticklebacks, Pungitius pungitius. Copeia, 1979, 405-412.
Hunt G, Bell MA, Travis MP (2008) Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution, 62, 700-710.
van Houdt JKJ, de Cleyn L, Perretti A, Volckaert FAM (2005) A mitogenic view on the evolutionary history of the Holarctic freshwater gadoid, burbot (Lota lota). Molecular Ecology, 14, 2445-2457.
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Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods), Version 4.0b10. Sinauer, Sunderland, MA, USA.
Colosimo PF, Hosemann KE, Balabhadra S et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science, 307, 1928-1933.
Orti G, Bell MA, Reimchen TE, Meyer A (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent migrations. Evolution, 48, 608-622.
Morris D (1958) The reproductive behaviour of the ten-spined stickleback (Pygosteus pungitius L.). Behaviour, Supplement, 1-154.
Herczeg G, Gonda A, Merila J (2009a) Evolution of gigantism in nine-spined sticklebacks. Evolution, 63, 3190-3200.
Bernatchez L (1997) Mitochondrial DNA analysis confirms the existence of two glacial races of rainbow smelt Osmerus mordax and their reproductive isolation in the St Lawrence River estuary (Quebec, Canada). Molecular Ecology, 6, 73-83.
McPhail JD (1963a) Geographic variation in North American ninespine sticklebacks, Pungitius pungitius. Journal of the Fisheries Research Board of Canada, 20, 27-44.
Shikano T, Shimada Y, Herczeg G, Merilä J (2010) History vs. habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations. Molecular Ecology, 19, 1147-1161.
Wootton RJ (1984) Functional Biology of Sticklebacks. University of California Press, Berkeley.
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
Larkin MA, Blackshields G, Brown NP et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
Ayvazian SG, Krueger WH (1992) Lateral plate ontogeny in the North American ninespine stickleback, Pungitius occidentalis. Copeia, 1992, 209-214.
Steiner CC, Weber JN, Hoekstra HE (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biology, 5, e219.
Curry RA (2007) Late glacial impacts on dispersal and colonization of Atlantic Canada and Maine by freshwater fishes. Quaternary Research, 67, 225-233.
Peichel CL, Nereng KS, Ohgi KA et al. (2001) The genetic architecture of divergence between threespine stickleback species. Nature, 414, 901-905.
Shapiro MD, Marks ME, Peichel CL et al. (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428, 717-723.
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a
1982; 56
2010; 98
2010; 19
1986; 33
1971; 1971
2006; 38
1993; 21
1983; 4
1996; 382
2008; 9
1995; 139
1976
1996; 144
1997; 6
1963a; 20
1995; 132
2003; 52
2005; 22
2007; 38
1997; 147
1983; 105
2009; 2009
2000; 18
2009; 96
2001
2000
2006; 22
1999; 16
1979; 1979
2000; 405
2007; 131
1994; 1994
1986
1967; 19
2005; 307
1981; 38
2007; 7
1984
2007; 5
2001; 55
2008; 62
2009; 19
2003; 40
2007; 67
2007; 23
1998; 55
2001; 414
1998; 14
2001; 10
1993; 47
2009; 22
2009; 63
2009b; 22
2009; 20
2010; 327
1965; 122
2009a; 63
2006; 15
1963b
2009
2008
2007
2006
1994
1994; 48
2000; 155
2002
1999; 8
2004; 428
2001; 21
1980; 58
2006; 40
1992; 131
1992; 1992
1958; Supplement
1955; 106
1878; 13
2008; 48
2008; 46
1992; 68
2009; 5
1998; 7
2006; 103
2005; 14
1964; 443
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Snippet The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene...
The current geographical distribution of the ninespine stickleback ( Pungitius pungitius ) was shaped in large part by the glaciation events of the Pleistocene...
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SubjectTerms anatomy & histology
Animals
Bayes Theorem
Biogeography
Cell Nucleus
Cell Nucleus - genetics
convergent evolution
DNA, Mitochondrial
DNA, Mitochondrial - genetics
East Asia
Ecology
Europe
Evolution, Molecular
Far East
fins
Fish
Genetic Variation
genetics
Genetics, Population
Geographical distribution
glacial refugia
Glaciation
Glaciers
Microsatellite Repeats
Mississippi
Mitochondrial DNA
Molecular biology
North America
phenotype
Phylogeny
Phylogeography
Pleistocene
population genetics-empirical
Pungitius
Pungitius pungitius
refuge habitats
Refugia
Sequence Analysis, DNA
skeleton
Smegmamorpha
Smegmamorpha - anatomy & histology
Smegmamorpha - genetics
stickleback
Title Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits
URI https://api.istex.fr/ark:/67375/WNG-MWRSW3XT-P/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1365-294X.2010.04801.x
https://www.ncbi.nlm.nih.gov/pubmed/20854276
https://www.proquest.com/docview/750432862
https://www.proquest.com/docview/1400118961
https://www.proquest.com/docview/755164300
https://www.proquest.com/docview/762282273
Volume 19
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