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High Frequency of Sex and Equal Frequencies of Mating Types in Natural Populations of the Ciliate Tetrahymena Thermophila F

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High Frequency of Sex and Equal Frequencies of Mating Types in Natural Populations of the Ciliate Tetrahymena Thermophila F Proc. Natl. Acad. Sci. USA Vol. 92, pp. 8715-8718, September 1995 Population Biology High frequency of sex and equal frequencies of mating types in natural populations of the ciliate Tetrahymena thermophila F. PAUL DOERDERt, MICHAEL A. GATES, FRANK P. EBERHARDT, AND MUHIrTIN ARSLANYOLU Department of Biology, Cleveland State University, Cleveland, OH 44115 Communicated by John R. Preer, Jr., Indiana University, Bloomington, IN, June 5, 1995 ABSTRACT In ciliate protists, sex involves the temporary To determine the incidence of sex and the frequencies of joining of two cells of compatible mating type, followed by multiple mating types in natural populations of Tetrahymena meiosis and exchange of gametic nuclei between conjugants. thermophila, we have extensively sampled ponds in which T. Reproduction is by asexual binary fission following conjuga- thermophila is resident. tion. For the many ciliates with fixed multiple mating types, frequency-dependent sex-ratio theory predicts equal frequen- MATERIALS AND METHODS cies of mating types, if sex is common in nature. Here, we report that in natural populations of Tetrahymena thermophila Study ponds are located in the Allegheny National Forest of sexually immature cells, indicative of recent conjugation, are northwestern Pennsylvania. Ponds are located 41.5° north found from spring through fall. In addition, the seven mating latitude, 78.9° longitude at -580 m above sea level and were types occur in approximately equal frequencies, and these constructed between 1950 and 1970. Ponds are spring fed, with frequencies appear to be maintained by interaction between the pH of the water ranging from 4.2 to 6.4. Samples of pond complex, multiple mat alleles and environmental conditions water (usually 150 ml but sometimes 30 ml) were collected and during conjugation. Such genotype-environment interaction placed in plastic bags in the field. Proteose peptone, penicillin determining mating type frequency is rare among ciliates. G, and streptomycin (0.1%, 3 mg/ml, and 3 mg/ml, respec- tively) were subsequently added to eliminate most nontetra- Sex is an extraordinarily successful eukaryotic invention usu- hymenine species. Two to three days later, bags were scored for ally associated with reproduction. However, in ciliates, repro- the presence of Tetrahymena-like cells, and from positive bags, duction is by binary fission, and sex is limited to the temporary 1-12 (usually 4) single cells were cloned into fresh medium conjugal union of two cells for purposes of recombination and [0.15% (wt/vol) cereal grass inoculated with Klebsiella pneu- rejuvenation-i.e., micronuclear exchange and macronuclear moniae]. Each clone was then tested for mating type (I-VII) and replacement. To recognize suitable partners, ciliates are dif- for the major cell surface immobilization serotype (Hi, H2, H3, ferentiated into mating types, a kind of self-not-self discrim- H4, J, K, or L) by standard procedures (11, 12). Mating-type ination system, as opposed to true sexes. Hurst and coworkers alleles were extracted in homozygous form by crossing isolates to (1, 2) have suggested that by exchanging only gametic nuclei at inbred genomic exclusion strain A*III (13, 14) to yield whole- conjugation, ciliates minimize conflict between cytoplasmic genome homozygotes (thus bypassing inbreeding). Genetically genomes and, therefore, are free to evolve multiple mating identical homozygotes were then crossed among themselves at types to maximize the choice of sexual partners. Simple 18°C, 28'C, and 37'C. After 3-10 fissions at the experimental extension of frequency-dependent sex-ratio theory suggests temperature (in which macronuclear development was complet- that multiple but fixed mating types should be equally frequent ed), cultures were returned to a constant 28'C, where a single cell in breeding populations, a suggestion supported by two theo- (karyonide) from each pair was serially transferred to sexual retical studies. Orias and Rohlf (3) constructed a deterministic maturity. Mating type was determined by mating each clone with model for three alleles at a single locus and found that there all seven mating type testers. is a stable equilibrium in which mating types are equally frequent. In a more general study, Iwasa and Sasaki (4) found RESULTS that evolutionary consequences greatly depend upon mating kinetics and sex-determining mechanisms. When opportuni- Ecological Distribution. T. thermophila is most commonly ties for finding suitable conjugal partners are temporally found in decaying vegetation at the mud-water interface and limited, the number of sexes-i.e., mating types-increases. in sympatry with other, unidentified Tetrahymena species (Fig. There is, however, limited information on ciliate sex and 1A). The frequency of positive samples varies directly with mating types in natural populations (5, 6) with which to test temperature, presumably as a consequence of bacterial food these models. supply. Ciliates typically have two types of nuclei: a germinal, Seasonal Distribution of Immature Isolates Indicating Re- diploid micronucleus capable of meiosis and mitosis and a cent Conjugation. The life cycle of T. thermophila includes an somatic, compound macronucleus controlling the phenotype immature phase after conjugation, during which cells are of the cell. At conjugation, haploid gametic nuclei meiotically unable to mate and therefore do not react with mating-type derived from the micronuclei are reciprocally exchanged, and, testers; the immaturity period typically is 60-100 fissions (15). following fertilization, new macronuclei are derived from Using T. thermophila-specific antisera (16), we were able to mitotic products of zygotic micronuclei, while the old macro- identify T. thermophila independent of the state of maturity nuclei are destroyed (7). Replacement of the macronucleus not (Fig. 1B). Immature cells, indicative of recent conjugation, only initiates a new life cycle that may include change in mating were found throughout the collecting season, with two appar- type but also is associated with rejuvenating (8) and heterotic ent peaks: one in late spring/early summer and one in late effects (9, 10). summer/early autumn. Because - 15-20 fissions elapsed be- tween collection and testing isolated clones for maturity, the shown in Fig. 1B are underestimates of the true The publication costs of this article were defrayed in part by page charge frequencies payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 8715 Downloaded by guest on September 26, 2021 8716 Population Biology: Doerder et al. Proc. Natl. Acad. Sci. USA 92 (1995) A B 0.7 -WTWs -Twm Ejthws Ethw 30 a [t'7-'92rz3 ] pond water daily air t .6 ... ...... F2 i. .. -a.o.5a)~~~~~~~~~2t:... E 0 -|-,Z f 420 E 0.3 - 04 °E~~~~~~~~~~~~3 .. ..i.. 150 C D~~~~~~~~~~~~ Apr May Jun Jul Aug Sep Oct Apr May Jun Jul Aug Sep Oct (916) (1334) (659) (916) (753) (744) (605) '87-|92: (57) (161) (237) (328) (163) (279) (0) 'As (20) (38) (31) (101) (100) (21) (24) 193: (5) (226) (166) (1409) (862) (540) (44) I 0.25 ...0.30 F-. _.2 ...... IL 'I 0.05- l ll t tIL 1Wlul o M lllilllSl"00 m CRWPEm343SE1 SG292 0G25 ....|S1MayEI1Jun..2.. EJiul BAugESep| --(1820) (1484) (1329)0.20i 3L(265) (118) (573) (184) (178) F E I IIll IV V V~~~~ ~ ~~lVll1 l0l 20 ........ a6mf610.5 r - - -mat-7/maf-7| 041!- Hg -- -----1 0 20.25 u 0.32 F1Yi8 E28 B371 f318E28 E3 (75) (185) (38) .......(70) (78) (101) FIG. 1. (A) Fraction of samples positive for the presence of Tetrahymena-like species (Tetrahymena) and fraction of positive samples containing T. thermophila (th) collected at the surface (ws) or at the bottom (wm) at depths of 15-30 cm. The number of samples is indicated in parentheses. Pond (i) and average daily high/low air (E) temperatures (for Warren, PA) are for 1987-1993. (B) Seasonal distribution of immature T thermophila isolates in 1987-1992 and 1993. All clones reacting with T thermophila-specific antisera were tested for mating type by using all seven mating types. Mature clones reacted with one or (usually) more mating-type testers. Immature clones failed to react with any of the testers. Randomly selected clones eventually became mature (10-100 fissions), confirming the validity of the method. The number of samples is indicated in parentheses. (C) Frequencies of mating types I-VII in three study ponds (bars, sample sizes in parentheses) and throughout the region (line, n = 5822). (D) Seasonal distribution of mating types in pond SG29. Sample sizes are shown in parentheses. (E and F) Effect of temperature on mating-type frequencies for mat-6 (E) and mat-7 (F) homozygotes. Temperatures were 18°C, 28°C, and 37°C. Sample size of karyonides is shown in parentheses. Line shows distribution of mating types in pond SG29. frequency of immaturity. Immature isolates required an ad- Samples also frequently yielded more than one mating type. ditional 10-50 fissions to become mature. The seasonal fre- For example, among 495 samples from which four or more quencies of immature isolates-e.g., >25%-indicate fre- clones were isolated, 211 (42.6%) contained two or more quent conjugation. mating types. As expected, samples with multiple mating types Equal Frequencies of Multiple Mating Types. Because were more common in July, when the density of T. thermophila mating-type frequencies determine the probability that two appears to be the highest. Among 87 bottom samples, from mature cells are compatible, we also have examined mating- which 12 clones were isolated, 63 (72.4%) contained four or type distribution among 5822 clones of T. thermophila isolated more mating types and 2 (2.3%) contained all seven mating from these ponds (Fig. 1C). All seven previously known mating types. Among 42 control (surface) samples, 23 (54.8%) con- types (15) were present in each pond sampled (including ponds tained four or more mating types.
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