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Apparent Selection Intensity for the Cytochrome Oxidase Subunit I Gene Varies with Mode of Reproduction in Echinoderms

Genetica volume 122, pages 115–125 (2004)Cite this article

Abstract

When most amino acid substitutions in protein-coding genes are slightly deleterious rather than selectively neutral, life history differences can potentially modify the effective population size or the selective regime, resulting in altered ratios of non-synonymous to synonymous substitutions among taxa. We studied substitution patterns for the mitochondrial cytochrome oxidase subunit I (COI) gene in a sea star genus (Leptasterias spp.) with an obligate brood-protecting mode of reproduction and small-scale population genetic subdivision, and compared the results to available COI sequences in nine other genera of echinoderms with pelagic larvae: three sea stars, five sea urchins and one brittle star. We predicted that this life history difference would be associated with differences in the ratio of non-synonymous (d N) to synonymous (d S) substitution rates. Leptasterias had a significantly greater d N/d S ratio (both between species and within species), a significantly smaller transition/transversion rate ratio, and a significantly lower average nucleotide diversity within species, than did the non-brooding genera. Other explanations for the results, such as altered mutation rates or selective sweeps, were not supported by the data analysis. These findings highlight the potential influence of reproductive traits and other life history factors on patterns of nucleotide substitution within and between species.

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References

  • Biermann, C. H., B. D. Kessing & S. R. Palumbi, 2003. Phylogeny and development of marine model species: strongylo-centrotid sea urchins. Evol. Dev. 5: 360–371.

    PubMed  Google Scholar 

  • Bohonak, A. J., 1999. Dispersal, gene flow, and population structure. Q. Rev. Biol. 74: 21–45.

    PubMed  Google Scholar 

  • Charlesworth, B., 1998. Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15: 538–543.

    PubMed  Google Scholar 

  • Charlesworth, D. & S. I. Wright, 2001. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11: 685–690.

    PubMed  Google Scholar 

  • Debenham, P., M. Brzezinski, K. Foltz & S. Gaines, 2000. Genetic structure of populations of the red sea urchin, Strongylocentrotus franciscanus. J. Exp. Mar. Biol. Ecol. 253: 49–62.

    PubMed  Google Scholar 

  • Eckert, G. L., 2003. Effects of the planktonic period on marine population fluctuations. Ecology 84: 372–383.

    Google Scholar 

  • Edmands, S., P. E. Moberg & R. S. Burton, 1996. Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar. Biol. 126: 443–450.

    Google Scholar 

  • Emlet, R. B., L. R. McEdward & R. R. Strathmann, 1987. Echinoderm larval ecology viewed from the egg, pp. 55–136 in Echinoderm Studies, Vol. 2, edited by M. Jangoux & J. M. Lawrence. A. A. Balkema, Rotterdam, The Nether-lands.

    Google Scholar 

  • Flowers, J. M., 1999. Discordant patterns of genetic and morphological variation and their implications for the taxonomy of Leptasterias subgenus Hexasterias of the North Pacific. MS Thesis, Louisiana State University, Baton Rouge.

    Google Scholar 

  • Flowers, J. M. & D. W. Foltz, 2001. Reconciling molecular systematics and traditional taxonomy in a species-rich clade of sea stars (Leptasterias subgenus Hexasterias ). Mar. Biol. 139: 475–483.

    Google Scholar 

  • Flowers, J. M., S. C. Schroeter & R. S. Burton, 2002. The recruitment sweepstakes has many winners: genetic evi-dence from the sea urchin Strongylocentrotus purpuratus. Evolution 56: 1445–1453.

    PubMed  Google Scholar 

  • Foltz, D. W., 2003. Invertebrate species with non-pelagic larvae have elevated levels of non-synonymous substitutions and reduced nucleotide diversities. J. Mol. Evol. 57: 607–612.

    PubMed  Google Scholar 

  • Foltz, D. W., W. B. Stickle, E. L. Campagnaro & A. E. Himel, 1996. Mitochondrial DNA polymorphisms reveal addi-tional genetic heterogeneity within the Leptasterias hexactis (Echinodermata: Asteroidea)species complex. Mar. Biol. 125: 569–578.

    Google Scholar 

  • Geyer, L. B. & S. R. Palumbi, 2003. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57: 1049–1060.

    PubMed  Google Scholar 

  • Graustein, A., J. M. Gaspar, J. R. Walters & M. F. Palopoli, 2002. Levels of DNA polymorphism vary with mating system in the Nematode genus Caenorhabditis. Genetics 161: 99–107.

    PubMed  Google Scholar 

  • Hamrick, J. L. & M. J. W. Godt, 1996. Effects of life history traits on genetic diversity in plant species. Phil. Trans. Roy. Soc. L. 351B: 1291–1298.

    Google Scholar 

  • Hart, M. W., 2002. Life history evolution and comparative developmental biology of echinoderms. Evol. Dev. 4: 62–71.

    PubMed  Google Scholar 

  • Hasegawa, M., Y. Cao & Z. Yang, 1998. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: non-synonymous/synonymous rate ratio is much higher within species than between species. Mol. Biol. Evol. 15: 1499–1505.

    PubMed  Google Scholar 

  • Hedrick, P. W., 1999. Highly variable loci and their interpreta-tion in evolution and conservation. Evolution 53: 313–318.

    Google Scholar 

  • Hrincevich, A. W., 2002. Patterns of nucleotide substitution within and among mitochondrial gene regions in sea stars (Leptasterias spp.). PhD dissertation, Louisiana State University, Baton Rouge (permanent URL: http: //etd. lsu. e-du: 8085/docs/available/etd-0120102-223858/).

  • Hrincevich, A. W., A. Rocha-Olivares & D. W. Foltz, 2000. Phylogenetic analysis of molecular lineages in a species-rich subgenus of sea stars (Leptasterias subgenus Hexasterias). Am. Zool. 40: 365–374.

    Google Scholar 

  • Hughes, A. L. & M. Nei, 1988. Pattern of nucleotide substitu-tion at major histocompatibility complex class-I loci reveals overdominant selection. Nature 335: 167–170.

    PubMed  Google Scholar 

  • Jarne, P. & T. Städler, 1995. Population genetic structure and mating system evolution in freshwater pulmonates. Exper-ientia 51: 482–497.

    Google Scholar 

  • Kinlan, B. P. & S. D. Gaines, 2003. Propagule dispersal in marine and terrestrial environments: a community perspec-tive. Ecology 84: 2007–2020.

    Google Scholar 

  • Kumar, S., K. Tamura, I. B. Jakobsen & M. Nei, 2001. MEGA2: molecular evolutionary genetics analysis soft-ware. Bioinformatics 17: 1244–1245.

    Article  PubMed  Google Scholar 

  • Landry, C., L. B. Geyer, Y. Arakaki, T. Uehara & S. R. Palumbi, 2003. Recent speciation in the Indo-West Paci c: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc. R. Soc. L. 270B: 1839–1847.

    Google Scholar 

  • Lessios, H. A., 1981. Divergence in allopatry: molecular and morphological differentiation between sea urchins separated by the Isthmus of Panama. Evolution 35: 618–634.

    Google Scholar 

  • Lessios, H. A., 2001. Molecular phylogeny of Diadema: system-atic implications, pp. 487–495 in Echinoderms 2000, edited by M. Barker. A. A. Balkema, Lisse, The Netherlands.

    Google Scholar 

  • Lessios, H. A. & C. W. Cunningham, 1990. Gametic incompat-ibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44: 933–941.

    Google Scholar 

  • Lessios, H. A. & J. S. Pearse, 1996. Hybridization and intro-gression between Indo-Paci c species of Diadema. Mar. Biol. 126: 715–723.

    Google Scholar 

  • Lessios, H. A., B. D. Kessing & J. S. Pearse, 2001. Population structure and speciation in tropical seas: Global phyloge-ography of the sea urchin Diadema. Evolution 55: 955–975.

    PubMed  Google Scholar 

  • Lessios, H. A., B. D. Kessing, D. R. Robertson & G. Paulay, 1999. Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53: 806–817.

    Google Scholar 

  • McCartney, M. A., G. Keller & H. A. Lessios, 2000. Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol. Ecol. 9: 1391–1400.

    PubMed  Google Scholar 

  • McGovern, T. M., 2002. Patterns of sexual and asexual repro-duction in the brittle star Ophiactis savignyi in the Florida Keys. Mar. Ecol. Prog. Ser. 230: 119–126.

    Google Scholar 

  • McMillan, W. O., R. A. Ra. & S. R. Palumbi, 1992. Population genetic consequences of developmental evolution in sea urchins (Genus Heliocidaris). Evolution 46: 1299–1312.

    Google Scholar 

  • Moberg, P. E. & R. S. Burton, 2000. Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar. Biol. 136: 773–784.

    Google Scholar 

  • Nachman, M. W., 1998. Deleterious mutations in animal mitochondrial DNA. Genetica 102/103: 61–69.

    Google Scholar 

  • Ohta, T., 1992. The nearly neutral theory of molecular evolution. Annu. Rev. Ecol. Syst. 23: 263–286.

    Google Scholar 

  • Palumbi, S. R., 1996. What can molecular genetics contribute to marine biogeography?An urchin 's tale. J. Exp. Mar. Biol. Ecol. 203: 75–92.

    Google Scholar 

  • Palumbi, S. R. & E. C. Metz, 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echi-nometra). Mol. Biol. Evol. 8: 227–239.

    PubMed  Google Scholar 

  • Palumbi, S. R., G. Grabowsky, T. Duda, L. Geyer & N. Tachino, 1997. Speciation and population genetic struc-ture in tropical Paci c sea urchins. Evolution 51: 1506–1517.

    Google Scholar 

  • Pannell, J. R. & B. Charlesworth, 2000. Effects of metapopu-lation processes on measures of genetic diversity. Phil. Trans. Roy. Soc. L. 355B: 1851–1864.

    Google Scholar 

  • Rand, D. M., 2001. The units of selection on mitochondrial DNA. Annu Rev. Ecol. Syst. 32: 415–448.

    Google Scholar 

  • Rand, D. M. & L. M. Kann, 1998. Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica 102/103: 393–407.

    Google Scholar 

  • Roy, M. S. & R. Sponer, 2001. The recent evolutionary history of Ophiactis savignyi (Echinodermata;Ophiuroidea), pp. 307–311 in Echinoderms 2000, edited by M. Barker. A. A. Balkema, Lisse, The Netherlands.

    Google Scholar 

  • Roy, M. S. & R. Sponer, 2002. Evidence of a human-mediated invasion of the tropical western Atlantic by the 'world 's most common brittlestar. 'Proc. R. Soc. L. 269B: 1017–1023.

    Google Scholar 

  • Rozas, J. & R. Rozas, 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174–175.

    PubMed  Google Scholar 

  • Schoen, D. J. & A. H. D. Brown, 1991. Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc. Natl Acad. Sci. 88: 4494–4497.

    PubMed  Google Scholar 

  • Schopf, T. J. & L. S. Murphy, 1973. Protein polymorphism of the hybridizing seastars Asterias forbesi and Asterias vulgaris and implications for their evolution. Biol. Bull. 145: 589–597.

    Google Scholar 

  • Skold, M., S. R. Wing & P. V. Mladenov, 2003. Genetic subdivision of a sea star with high dispersal capability in relation to physical barriers in a fjordic seascape. Mar. Ecol. Prog. Ser. 250: 163–174.

    Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    PubMed  Google Scholar 

  • Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25: 4876–4882.

    Article  PubMed  Google Scholar 

  • Wang, J. & A. Caballero, 1999. Developments in predicting the effective size of subdivided populations. Heredity 82: 212–226.

    Google Scholar 

  • Ward, R. D. & J. Andrew, 1995. Population genetics of the northern Pacific seastar Asterias amurensis (Echinodermata: Asteriidae): allozyme differentiation among Japanese, Rus-sian, and recently introduced Tasmanian populations. Mar. Biol. 124: 99–109.

    Google Scholar 

  • Wares, J. P., 2001. Biogeography of Asterias: North Atlantic climate change and speciation. Biol. Bull. 201: 95–103.

    PubMed  Google Scholar 

  • Waters, J. M. & M. S. Roy, 2003. Global phylogeography of the ssiparous sea-star genus Coscinasterias. Mar. Biol. 142: 185–191.

    Google Scholar 

  • Watts, R. J., M. S. Johnson & R. Black, 1990. Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in western Australia. Mar. Biol. 105: 145–151.

    Google Scholar 

  • Whitlock, M. C., 2003. Fixation probability and time in subdivided populations. Genetics 164: 767–779.

    PubMed  Google Scholar 

  • Williams, S. T., 2000. Species boundaries in the star sh genus Linckia. Mar. Biol. 136: 137–148.

    Google Scholar 

  • Williams, S. T. & J. A. H. Benzie, 1996. Genetic uniformity of widely separated populations of the coral reef star sh Linckia laevigata from the East Indian and West Pacific Oceans, revealed by allozyme electrophoresis. Mar. Biol. 126: 99–107.

    Google Scholar 

  • Williams, S. T. & J. A. H. Benzie, 1997. Indo-West Pacific patterns of genetic differentiation in the high-dispersal star sh Linckia laevigata. Mol. Ecol. 6: 559–573.

    Google Scholar 

  • Yang, Z., 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555–556.

    PubMed  Google Scholar 

  • Yang, Z. & A. D. Yoder, 1999. Estimation of the transition/ transversion rate bias and species sampling. J. Mol. Evol. 48: 274–283.

    PubMed  Google Scholar 

  • Zigler, K. S., E. C. Ra., E. Popodi, R. A. Ra. & H. A. Lessios, 2003. Adaptive evolution of Bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57: 2293–2302.

    PubMed  Google Scholar 

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  1. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA

    David W. Foltz, Adam W. Hrincevich & Axayácatl Rocha-Olivares

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  1. David W. Foltz
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  2. Adam W. Hrincevich
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  3. Axayácatl Rocha-Olivares
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Correspondence to Axayácatl Rocha-Olivares.

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Foltz, D.W., Hrincevich, A.W. & Rocha-Olivares, A. Apparent Selection Intensity for the Cytochrome Oxidase Subunit I Gene Varies with Mode of Reproduction in Echinoderms. Genetica 122, 115–125 (2004). https://doi.org/10.1023/B:GENE.0000041002.97173.1e

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  • DOI: https://doi.org/10.1023/B:GENE.0000041002.97173.1e

  • brittle stars
  • cytochrome oxidase subunit I gene
  • echinoderms
  • mitochondrial DNA
  • sea stars
  • sea urchins
  • synonymous–non-synonymous substitution rate ratio

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