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Concerted Evolution at the Population Level: Pupfish Hindill Satellite DNA Sequences JOHN F

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Concerted Evolution at the Population Level: Pupfish Hindill Satellite DNA Sequences JOHN F Proc. Nati. Acad. Sci. USA Vol. 91, pp. 994-998, February 1994 Evolution Concerted evolution at the population level: Pupfish HindIll satellite DNA sequences JOHN F. ELDER, JR.* AND BRUCE J. TURNER Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Communicated by Bruce Wallace, October 18, 1993 ABSTRACT The canonical monomers (170 bp) of an organisms. There are very little data on their variation within abundant (1.9 x 10' copies per diploid genome) satellite DNA or divergence among conspecific natural populations. sequence family In the genome of Cyprinodon wriegau, a We report here sequence comparisons ofthe predominant "pph" that ranges along the Atlantic coast fom Cape Cod or "canonical" monomers of a satellite DNA array in sam- to central Mexico, are divergent in base sequence in 10 of 12 ples of 12 natural populations of Cyprinodon variegatus smle collected from natural populations. The divergence (Cyprinodontidae), a coastal killifish species. Ten of these Involves sbsitions, deletis, and insertions, is marked in samples have distinctive and characteristic canonical mono- scoe (mean pairwise sequence slarit = 61.6%; range = mers with high levels of intraindividual and intrapopulation 35-95.9%), Is largely ed to the 3' half of the monomer, homogeneity.t In other words, this satellite DNA has appar- and Is not correlated with the disace among cllg sites. ently undergone concerted evolution at or near the level of Repetitive loning and direct genomic sequencing expriments the local population. failed to detect intrapopulation and intraindividual variation, A preliminary account of some of our early findings has hig levels of sequence homogeneity within popu- appeared in a symposium volume (6). latios. The satellite s has therefore undergone "con- certed evolution," at the level of the local population. Con- certed evolution has previously almost always been dsused in MATERIALS AND METHODS terms of the divergence of species or higher taxa; its intraspe- Organism and Samples. C. variegatus Lacepede, some- cific occurnce apparently has not been reported previously. times called the "Sheepshead minnow," is a common, in- The gnerality of the observation is difficult to evaluate, for shore, euryhaline, "pupfish" species that ranges from Cape altough Esatellite DNAs fom a large number oforganisms have Cod, MA, to the mouth ofthe Rio Tuxpan, Mexico. Related, been su ied In detail, there appear to be little or no other data sometimes morphologically divergent, populations exist in on their sequence variaton in natural populations. The rela- some Floridian freshwater lakes, Yucatan/Belize, Bahamas, tionp (if any) between concerted, population level, satellite several Caribbean islands, and coastal Venezuela (7, 8). Most DNA divergence and the eatent of gene flow/genetic Iolation specialists would agree that its distribution is "patchy" among conspeiflc natural populations remains to be estab- throughout its range-i.e., it is locally (and sometimes sea- lished. sonally) abundant in appropriate habitats. However, little else is known of its population structure, dynamics, or local Comparisons ofparalogous repetitive DNA sequences in the genetic contiguity. It was selected for further study from an genomes of eukaryotes often reveal striking intraspecific initial restriction enzyme survey of satellite DNAs in 20-30 similarities but marked interspecific divergences. This ap- fish species (B.J.T., unpublished data) because ofthe appar- parent evolutionary nonindependence of the members of a ent simplicity ofits satellite monomers and its abundance and sequence family is termed "concerted evolution" (1). The ease of sampling. Samples are detailed in Fig. 1. Sampling forces that mediate concerted evolution are believed to locations were determined solely by convenience and the include biased gene conversion, unequal crossing-over, and field activities of colleagues and do not reflect any putative replicative transposition (2). The term "molecular drive" (2) subdivisions within the species. Two to nine pUC19 clones is sometimes used to describe these forces acting together were sequenced from 1-5 specimens per site. HindIII ge- with stochastic population events (genetic drift, founder nomic bands were directly sequenced (see below) from 5-12 effects, etc.). specimens per site (depending on sample size). The significance ofmolecular drive or its component forces DNA Preparations and Detection/Cloning of Satellite Se- at the population level is currently unknown. Some theoret- quences. Genomic DNA was purified from homogenates of ical studies (e.g., ref. 3) suggest that it could be important in whole fish (less scales, skin, and gut) in 4 M guanidinium promoting the divergence of conspecific populations in a isothiocyanate, followed by phenol/chloroform and chloro- non-Darwinian manner. However, this intriguing notion is form extractions, as described (9). Presumptive satellite currently without empirical support, for there appear to be no sequences were detected as coherent bands upon agarose gel published examples of interpopulation (but intraspecific) electrophoresis of HindIII or Sst I digests of genomic DNA. concerted evolution. Only the HindIll satellite is discussed here. Bands were Highly repetitive, tandemly arrayed, "satellite" DNAs are excised from low-melting agarose; purification and ligation general features of eukaryotic genomes (4). These sequence into the HindIII cloning site of plasmid pUC19 followed families often provide clear-cut examples of interspecific standard methods (10, 11). concerted evolution (e.g., ref. 5). Most satellite DNAs have Genomic Copy Number and Hybridization Experiments. been characterized only from laboratory strains, cell lines, or Satellite copy number was estimated by hybridization of a limited (and frequently pooled) sample of field-caught *To whom reprint requests should be sent at the present address: Department of Biology, University of North Dakota, P.O. Box The publication costs ofthis article were defrayed in part by page charge 8238, University Station, Grand Forks, ND 58202. payment. This article must therefore be hereby marked "advertisement" *The sequences reported in this paper have been deposited in the in accordance with 18 U.S.C. §1734 solely to indicate this fact. GenBank data base (accession nos. U02331-U02340). 994 Downloaded by guest on October 1, 2021 Evolution: Elder and Turner Proc. Natl. Acad. Sci. USA 91 (1994) 995 0 100 240 i- i I ---- kilometer 50 150 FIG. 1. C. variegatus population samples and locations. 1A, Cape Cod, MA, site I (north shore, Buzzard's Bay) (3 specimens); 1B, Cape Cod, MA, site II (Oyster Pond, Woods Hole) (7 specimens); 2, Hereford Inlet, NJ (12 specimens); 3, Lusby, MD (Patuxent R. at Drum Point Lake) (15 specimens); 4, Sapelo Island, GA, two proximate stations: site I (west side of island) (16 specimens) and site II (Light House Ditch) (16 specimens); 5, Jacksonville, FL (Forest Street culvert) (12 specimens); 6, Tampa Bay, FL, site I (Pinellas Pt.) (20 specimens); 7, Tampa Bay, site II (Port Manatee) (12 specimens); 8, Key West, FL (8 specimens); 9, New Orleans, LA (Lake Pontchartrain) (8 specimens); 10, High Island, TX (intercoastal waterway bridge) (5 specimens). cloned monomer to a dilution series of slot-blotted genomic monomer (see below). The Vent (exo-) cycle sequencing DNAs. Signal intensities were compared to those generated system (New England Biolabs) was used with the 35S incor- by known amounts of purified satellite monomer applied to poration protocol recommended by the manufacturer, except the same membrane (12). Cross-reaction of C. variegatus that a single initial denaturation period of 5 min at 950C was HindIII satellite monomer with sequences in the genomes of used, followed by 40 cycles of950C for 30 sec, 650C for 30 sec, other fish species was also assessed by slot blot hybridiza- and 750C for 30 sec. The superior thermostability of Vent tion. In all such experiments, probes were radiolabeled (32p) (exo-) tm polymerase allowed the use of very high temper- by random oligonucleotide priming (13). Nylon membranes atures during the sequencing reactions; this resulted in the (Zeta-Probe, Bio-Rad) were prehybridized in 50%o forma- elimination ofsome "stop" sequencing artifacts, presumably = due to template secondary structure, which were visible mide, 1% SDS, 4x SSPE (lx SSPE 0.18 M NaCl/10 mM when Taq polymerase was used in initial experiments. sodium phosphate/i mM EDTA), 0.5 mg of tRNA per ml, Direct sequence comparisons of cloned monomers and and 0.5% Blotto at 42TC. Hybridization was allowed to genomic monomer fractions were made by excising the proceed overnight at the same temperature and in the same cloned monomers from recombinant plasmids, purifying solution but with 10%6 dextran sulfate and 106 cpm of probe them by gel electrophoresis, and then using them as tem- added per ml ofhybridization fluid. Membranes were rinsed, plates in Vent (exo-) tm cycle sequencing reactions. These at room temperature, consecutively for 15-min periods in 2x employed an identical protocol to, and were conducted SSC, 0.5x SSC, and O.lx SSC (all made 0.1% in SDS; lx simultaneously with, genomic sequencing reactions. The SSC = 0.15 M NaCl/15 mM sodium citrate); the final wash sequences of cloned and genomic monomer fractions from was for 30 min at 50TC in O.lx SSC/1% SDS. the same individual or population were then compared side- Sequencing of Cloned Monomers. Satellite monomers by-side on "Long
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