ACCELERATED MOLECULAR EVOLUTION IN HALOPHILIC CRUSTACEANS

Abstract In contrast to the stable ionic composition of the oceans, inland waters show striking diversity, possessing salt concentrations varying from 1 mM to 5 M. Although species diversity is highest in fresh water, some lineages have colonized hypersaline environments where they encounter elevated levels of both ultraviolet (UV) radiation and osmotic stress. This study compares rates of evolution in halophilic and freshwater taxa for two groups of microcrustaceans, anostracans and daphniids, from Australia and North America. The results establish that halophilic species show consistent rate acceleration, involving elevated levels of both insertion/deletion events and of nucleotide substitutions. The elevated pace of molecular evolution does not appear to be linked to selection or to other agents that are known to influence the supply rate of mutations, such as UV exposure, generation length, or shifts in metabolic rate. However, variance in ionic strength, which is known to have potent effects on DNA-protein interactions as well as on the structural properties of DNA and proteins, might account for the lowered fidelity of DNA replication in life from hypersaline settings. Regardless of its cause, the consistent rate acceleration in halophiles suggests that past efforts to employ sequence divergences to date events, such as the age of asexual lineages in Artemia, have resulted in serious overestimates. More generally, the results indicate that coordinated shifts in rates of molecular evolution may occur in lineages exposed to extreme environmental conditions. Corresponding Editor: H. Ochman

[1]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[2]  R. Marco,et al.  The complete mitochondrial DNA sequence of the crustacean Artemia franciscana , 1994, Journal of Molecular Evolution.

[3]  J. A. Bray,et al.  Interdomain linkage in the polymeric hemoglobin molecule of Artemia , 1994, Journal of Molecular Evolution.

[4]  R. Marco,et al.  Speciation in the Artemia genus: Mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps , 1994, Journal of Molecular Evolution.

[5]  M. Hasegawa,et al.  Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: Rapid evolution in warm-blooded vertebrates , 1993, Journal of Molecular Evolution.

[6]  P. Deckker Australian salt lakes: their history, chemistry, and biota — a review , 1983, Hydrobiologia.

[7]  M. Geddes 14. The brine shrimps Artemia and Parartemia , 1981, Hydrobiologia.

[8]  R. Kaplan Evolutionary adjustment of spontaneous mutation rates , 2004, Humangenetik.

[9]  Paul Baumann,et al.  Faster evolutionary rates in endosymbiotic bacteria than in cospeciating insect hosts , 2004, Journal of Molecular Evolution.

[10]  P. Hebert,et al.  Phylogenetic relationships and remarkable radiation in Parartemia (Crustacea: Anostraca), the endemic brine shrimp of Australia: evidence from mitochondrial DNA sequences☆ , 2001 .

[11]  B. Collette,et al.  Phylogenetic Relationships of New World Needlefishes (Teleostei: Belonidae) and the Biogeography of Transitions between Marine and Freshwater Habitats , 2001, Copeia.

[12]  Sudhir Kumar,et al.  Efficiency of the Neighbor-Joining Method in Reconstructing Deep and Shallow Evolutionary Relationships in Large Phylogenies , 2000, Journal of Molecular Evolution.

[13]  P. Hebert,et al.  Affinities among anostracan (Crustacea: Branchiopoda) families inferred from phylogenetic analyses of multiple gene sequences. , 2000, Molecular phylogenetics and evolution.

[14]  K. Klenin,et al.  The diameter of the DNA superhelix decreases with salt concentration: SANS measurements and Monte Carlo simulations , 2000 .

[15]  P. Hebert,et al.  Diversity of the genus Daphniopsis in the saline waters of Australia , 2000 .

[16]  R. Escalante,et al.  High DNA sequence variability at the alpha 1 Na/K-ATPase locus of Artemia franciscana (brine shrimp): polymorphism in a gene for salt-resistance in a salt-resistant organism. , 2000, Molecular biology and evolution.

[17]  T. Spears,et al.  BRANCHIOPOD MONOPHYLY AND INTERORDINAL PHYLOGENY INFERRED FROM 18S RIBOSOMAL DNA , 2000 .

[18]  M. Tristem Molecular Evolution — A Phylogenetic Approach. , 2000, Heredity.

[19]  T. Crease The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). , 1999, Gene.

[20]  Teresa J. Crease,et al.  Phylogenetic evidence for a single long-lived clade of crustacean cyclic parthenogens and its implications for the evolution of sex , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  Yves Van de Peer,et al.  Database on the structure of small subunit ribosomal RNA , 1999, Nucleic Acids Res..

[22]  T. Crease,et al.  The origin and evolution of variable-region helices in V4 and V7 of the small-subunit ribosomal RNA of branchiopod crustaceans. , 1998, Molecular biology and evolution.

[23]  C. Cockell Biological effects of high ultraviolet radiation on early earth--a theoretical evaluation. , 1998, Journal of theoretical biology.

[24]  M. Willson,et al.  FISHES AND THE FOREST , 1998 .

[25]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[26]  C. Marshall,et al.  The Coming of Age of Molecular Systematics , 1998, Science.

[27]  M. Pagel,et al.  Accelerated evolution as a consequence of transitions to mutualism. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[28]  F. Taddei,et al.  Role of mutator alleles in adaptive evolution , 1997, Nature.

[29]  M. Gouy,et al.  Extreme differences in rates of molecular evolution of foraminifera revealed by comparison of ribosomal DNA sequences and the fossil record. , 1997, Molecular biology and evolution.

[30]  D Penny,et al.  Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence , 1997, Science.

[31]  Y Van de Peer,et al.  Database on the structure of large ribosomal subunit RNA. , 1997, Nucleic acids research.

[32]  Yves Van de Peer,et al.  Database on the structure of small ribosomal subunit RNA , 1998, Nucleic Acids Res..

[33]  W. Rudin,et al.  Salt-dependent performance variation of DNA polymerases in co-amplification PCR. , 1996, BioTechniques.

[34]  N. Moran Accelerated evolution and Muller's rachet in endosymbiotic bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  P. Hebert,et al.  The systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  K. Kuma,et al.  Evolution of gene families and relationship with organismal evolution: rapid divergence of tissue-specific genes in the early evolution of chordates. , 1996, Molecular biology and evolution.

[37]  O P Judson,et al.  Ancient asexual scandals. , 1996, Trends in ecology & evolution.

[38]  H. Matsuda,et al.  Nucleotide substitution type dependence of generation time effect of molecular evolution. , 1995, Idengaku zasshi.

[39]  A. Feduccia Explosive Evolution in Tertiary Birds and Mammals , 1995, Science.

[40]  S. Conway Morris Ecology in deep time. , 1995, Trends in ecology & evolution.

[41]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[42]  P. Hebert,et al.  PROVINCIALISM IN PLANKTON: ENDEMISM AND ALLOPATRIC SPECIATION IN AUSTRALIAN DAPHNIA , 1994, Evolution; international journal of organic evolution.

[43]  M. Steel,et al.  Recovering evolutionary trees under a more realistic model of sequence evolution. , 1994, Molecular biology and evolution.

[44]  D. Lilley,et al.  Large-scale opening of A + T rich regions within supercoiled DNA molecules is suppressed by salt. , 1994, Nucleic acids research.

[45]  D. Thaler The evolution of genetic intelligence. , 1994, Science.

[46]  D. Rand Thermal habit, metabolic rate and the evolution of mitochondrial DNA. , 1994, Trends in ecology & evolution.

[47]  P. Hainaut,et al.  Increased salt concentration reversibly destabilizes p53 quaternary structure and sequence-specific DNA binding. , 1994, The Biochemical journal.

[48]  Orlandini,et al.  Knotting and supercoiling in circular DNA: A model incorporating the effect of added salt. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[49]  N. Moran,et al.  A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  P. Hebert,et al.  A TAXONOMIC REEVALUATION OF NORTH AMERICAN DAPHNIA (CRUSTACEA: CLADOCERA).III. THE D. CATAWBA COMPLEX , 1993 .

[51]  A. Ziegler,et al.  Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Andrew P. Martin,et al.  Body size, metabolic rate, generation time, and the molecular clock. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[53]  A B Smith,et al.  Comparative variation of morphological and molecular evolution through geologic time: 28S ribosomal RNA versus morphology in echinoids. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[54]  T. Ohta THE NEARLY NEUTRAL THEORY OF MOLECULAR EVOLUTION , 1992 .

[55]  J. Simon,et al.  A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[56]  M. Record,et al.  Analysis of equilibrium and kinetic measurements to determine thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA. , 1991, Methods in enzymology.

[57]  J. Gillespie The causes of molecular evolution , 1991 .

[58]  P. Herbert,et al.  The Adaptive Significance of Cuticular Pigmentation in Daphnia , 1990 .

[59]  R. Cole,et al.  Chromatin aggregation depends on the anion species of the salts. , 1989, The Journal of biological chemistry.

[60]  B. D. Davis,et al.  Transcriptional bias: a non-Lamarckian mechanism for substrate-induced mutations. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[61]  John M. Hancock,et al.  Complete sequences of the rRNA genes of Drosophila melanogaster. , 1988, Molecular biology and evolution.

[62]  M C Mossing,et al.  Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression. , 1987, The Journal of biological chemistry.

[63]  E. Moriyama Higher rates of nucleotide substitution in Drosophila than in mammals , 1987 .

[64]  P. Hebert,et al.  Ecological and Physiological Differentiation Among Low‐Artic Clones of Daphnia Pulex , 1987 .

[65]  M W Feldman,et al.  Modifiers of mutation rate: a general reduction principle. , 1986, Theoretical population biology.

[66]  G. Volckaert,et al.  Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. , 1984, Nucleic acids research.

[67]  L. E. Fox The removal of dissolved humic acid during estuarine mixing , 1983 .

[68]  M. E. Clark,et al.  Living with water stress: evolution of osmolyte systems. , 1982, Science.

[69]  M. Geddes The brine shrimps Artemia and Parartemia , 1981 .

[70]  M. Goulding,et al.  The Fishes and the Forest , 2023 .

[71]  N. Hairston Photoprotection by carotenoid pigments in the copepod Diaptomus nevadensis. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Leigh Eg,et al.  The evolution of mutation rates. , 1973 .

[73]  H. Berger,et al.  Selective allele loss in mixed infections with T4 bacteriophage. , 1973, Genetics.

[74]  E. Leigh,et al.  The evolution of mutation rates. , 1973, Genetics.

[75]  W. Burns,et al.  Comparative Animal Physiology , 1953, Nature.

[76]  L. F. Nims Osmotic Regulation in Aquatic Animals , 1939, The Yale Journal of Biology and Medicine.