Ciliate mating systems are highly diversified, providing unique opportunities to study sexual differentiation and its implications for mating dynamics. Many species of ciliates have multiple (>2) sexes. More sexes may mean more choice and an opportunity for evolution of preferential mating. We asked if the multiple sexes of the ciliate Tetrahymena thermophila mate preferentially among each other. We quantified pairing frequencies among four sexes of T. thermophila using experiments that allowed the sexes to compete as mating partners. We found that all sexes mated equally frequently among each other, that is, we found no evidence of preferential mating with respect to sex. This suggests that the “mate choice” in this ciliate is binary, between whether to form a pair or not and, in this regard, sex facilitates only self-/non-self-distinction. Thus, presence of multiple sexes does not necessarily result in the evolution of mating bias, which could decrease the maximum amount of mating that would otherwise be possible in a population. Our result of random mating verifies a key assumption in the theoretical model of sex ratio evolution in T. thermophila. Investigation into molecular differences between the sexes will be necessary to reveal the mechanistic basis of random mating among them. 1. Introduction Mating is random when two individuals in a population are just as likely as any other two individuals to mate. Evolution of mating preferences requires that potential mates are differentially attractive. Thus, random mating is expected if there is little variance in the perceived “quality” of mates. In natural populations, mating is rarely random [1]. Nonrandom mating results when individuals tend to choose mates with a specific phenotype and the associated genotype(s) among compatible mates. Dynamics of nonrandom mating have been studied in sexually dimorphic species in which size, sound, and color often describe the most preferred phenotype [2]. Among the microbial eukaryotes, mate-preference has been demonstrated in the yeast Saccharomyces cerevisiae, in which the highest amount of pheromone produced defines the most preferred phenotype for the cells of either sex [3]. It is largely unclear how mates are chosen in other unicellular organisms. Often, unicellular species have more than two sexes, raising an obvious yet previously unanswered question: do more sexes mean more choice, thereby making evolution of mate preference among the sexes inevitable? In other words, is selective mating observed when there is an opportunity to choose between many
References
[1]
L. Partridge, “Non-random mating and offspring fitness,” in Mate Choice, pp. 227–253, Cambridge University Press, Cambridge, UK, 1983.
[2]
M. B. Andersson, Sexual Selection, Princeton University Press, 1994.
[3]
C. L. Jackson and L. H. Hartwell, “Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal,” Cell, vol. 63, no. 5, pp. 1039–1051, 1990.
[4]
D. L. Nanney and E. M. Simon, “Laboratory and evolutionary history of Tetrahymena thermophila,” Methods in Cell Biology, no. 62, pp. 3–25, 2000.
[5]
M. J. Finley and P. J. Bruns, “Costimulation in Tetrahymena. II. A nonspecific response to heterotypic cell-cell interactions,” Developmental Biology, vol. 79, no. 1, pp. 81–94, 1980.
[6]
E. Orias, “Probable somatic DNA rearrangements in mating type determination in Tetrahymena thermophila: a review and a model,” Developmental Genetics, vol. 2, no. 2, pp. 185–202, 1981.
[7]
A. Miyake, “Fertilization and sexuality in ciliates,” in Ciliates: Cells as Organisms, K. Hausmann and P. Bradbury, Eds., pp. 243–290, Gustav Fischer, Stuttgart, Germany, 1996.
[8]
B. Love and M. B. Rotheim, “Cell surface interactions in conjugation: Tetrahymena ciliary membrane vesicles,” Molecular and Cellular Biology, vol. 4, no. 4, pp. 681–687, 1984.
[9]
Y. Iwasa and A. Sasaki, “Evolution of the number of sexes,” Evolution, vol. 41, pp. 49–65, 1987.
[10]
H. A. Murphy, H. A. Kuehne, C. A. Francis, and P. D. Sniegowski, “Mate choice assays and mating propensity differences in natural yeast populations,” Biology Letters, vol. 2, no. 4, pp. 553–556, 2006.
[11]
J. Y. Leu and A. W. Murray, “Experimental evolution of mating discrimination in budding yeast,” Current Biology, vol. 16, no. 3, pp. 280–286, 2006.
[12]
P. J. Bruns and D. Cassidy-Hanley, “Methods for genetic analysis,” Methods in Cell Biology, no. 62, pp. 229–240, 2000.
[13]
S. L. Allen, “Genomic exclusion: a rapid means for inducing homozygous diploid lines in Tetrahymena pyriformis, syngen,” Science, vol. 155, no. 3762, pp. 575–577, 1967.
[14]
L. K. Bleyman, M. P. Baum, P. J. Bruns, and E. Orias, “Mapping the mating type locus of Tetrahymena thermophila: meiotic linkage of mat to the ribosomal RNA gene,” Developmental Genetics, vol. 13, no. 1, pp. 34–40, 1992.
[15]
M. A. Virtue and E. S. Cole, “A cytogenetic study of development in mechanically disrupted pairs of Tetrahymena thermophila,” Journal of Eukaryotic Microbiology, vol. 46, no. 6, pp. 597–605, 1999.
[16]
E. P. Hamilton and E. Orias, “Genetic crosses: setting up crosses, testing progeny, and isolating phenotypic assortants,” Methods in Cell Biology, no. 62, pp. 219–228, 2000.
[17]
E. A. Spangler and E. H. Blackburn, “The nucleotide sequence of the 17 S ribosomal RNA gene of Tetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin,” Journal of Biological Chemistry, vol. 260, no. 10, pp. 6334–6340, 1985.
[18]
M. Ares and P. J. Bruns, “Isolation and genetic characterization of a mutation affecting ribosomal resistance to cycloheximide in Tetrahymena,” Genetics, vol. 90, no. 3, pp. 463–474, 1978.
[19]
P. J. Bruns, A. L. Katzen, L. Martin, and E. H. Blackburn, “A drug-resistant mutation in the ribosomal DNA of Tetrahymena,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 9, pp. 2844–2846, 1985.
[20]
B. C. Byrne, T. B. Brussard, and P. J. Bruns, “Induced resistance to 6-methylpurine and cycloheximide in Tetrahymena. I. Germ line mutants of T. thermophila,” Genetics, vol. 89, no. 4, pp. 695–702, 1978.
[21]
E. Cole, “The Tetrahymena conjugation junction—Madame Curie Bioscience Database—NCBI Bookshelf,” 2000, In Madame Curie Bioscience, http://www.ncbi.nlm.nih.gov/books/NBK6002/.
[22]
P. Luporini, C. Alimenti, C. Ortenzi, and A. Vallesi, “Ciliate mating types and their specific protein pheromones,” Acta Protozoologica, vol. 44, no. 2, pp. 89–101, 2005.
[23]
C. J. Maclean and D. Greig, “Prezygotic reproductive isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus,” BMC Evolutionary Biology, vol. 8, article 1, 2008.
[24]
L. A. Katz, O. Snoeyenbos-West, and F. P. Doerder, “Patterns of protein evolution in Tetrahymena thermophila: implications for estimates of effective population size,” Molecular Biology and Evolution, vol. 23, no. 3, pp. 608–614, 2006.
[25]
P. Doerder, M. A. Gates, F. P. Eberhardt, and M. Arslanyolu, “High frequency of sex and equal frequencies of mating types in natural populations of the ciliate Tetrahymena thermophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 19, pp. 8715–8718, 1995.
[26]
F. P. Doerder, M. Arslanyolu, Y. Saad, M. Kaczmarek, M. Mendoza, and B. Mita, “Ecological genetics of Tetrahymena thermophila: mating types, i-antigens, multiple alleles and epistasis,” Journal of Eukaryotic Microbiology, vol. 43, no. 2, pp. 95–100, 1996.
[27]
M. A. Gates, “Morphological drift accompanying nascent population differentiation in the ciliate Euplotes vannus,” Journal of Protozoology, vol. 37, no. 2, pp. 78–86, 1990.
[28]
J. W. Busch and D. J. Schoen, “The evolution of self-incompatibility when mates are limiting,” Trends in Plant Science, vol. 13, no. 3, pp. 128–136, 2008.
[29]
S. S. Phadke and R. A. Zufall, “Rapid diversification of mating systems in ciliates,” Biological Journal of the Linnean Society, vol. 98, no. 1, pp. 187–197, 2009.
[30]
T. Paix？o, S. S. Phadke, R. B. R. Azevedo, and R. A. Zufall, “Sex ratio evolution under probabilistic sex determination,” Evolution, vol. 65, no. 7, pp. 2050–2060, 2011.
