Is Evolution of Mating Preferences Inevitable? Random Mating in the Multisex System ofTetrahymena thermophila

Abstract

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.

Origins of Eukaryotic Sexual Reproduction

“…In most modern eukaryotes, this handicap has been assuaged by the evolution of countless systems for identifying the opposite type via pheromones and mating behaviors, enhancing the efficiency of finding a mate, but options are still limited to half the population. In some lineages, the odds have been improved by the presence of multiple mating types-three or more in Dictyostelium (Bloomfield et al 2010(Bloomfield et al , 2011, seven in Tetrahymena (Phadke et al 2012;Cervantes et al 2013;Umen 2013), 13 in Physarum polycephalum (Collins and Tang 1977;Clark and Haskins 2010), and often thousands in the basidiomycetes (Raper 1966)-and in these cases more encounters are sexually fertile (.98% in some basidiomycetes). But more outcrossing is not always better, and in basidiomycete fungi there are multiple independent transitions from the tetrapolar outcrossing species with thousands of sexes back to bipolar species with just two mating types, where it has been suggested that different environments favor outcrossing versus inbreeding sexual cycles ).…”

Molecular Polymorphism in the MTA and MTB Mating Type Genes of Tetrahymena thermophila and Related Asexual Species

“…However, our tests were not quantitative, and it is possible, though unlikely (Phadke et al. ), that differences in mating efficiency exist. More specific indicators of relatively weak purifying selection (Table ) include consistently negative values of Tajima's D, average K a / K s ratios of < 1 with significance at the 5% level, and, similarly, low π a / π s ratios.…”

“…Most amino acid substitutions involve those with similar functional groups, and, of course, cell lines with these substitutions were identified as mating types V or VII because each mated with sufficient vigor with 6/7 mating type testers to determine mating type. However, our tests were not quantitative, and it is possible, though unlikely (Phadke et al 2012), that differences in mating efficiency exist. More specific indicators of relatively weak purifying selection (Table 3) include consistently negative values of Tajima's D, average K a /K s ratios of < 1 with significance at the 5% level, and, similarly, low p a /p s ratios.…”

“…Moreover, mating types specified by mat 2 form pairs with equal efficiency, suggesting the choice of mating partner is random and opportunistic (Phadke et al. ). However, sex itself is a brief portion, typically 12–18 h depending on temperature, of a life cycle consisting of conjugation followed by reproduction by binary fission.…”

Ciliates learn to diagnose and correct classical error syndromes in mating strategies

“…Making mate choices based on the perceived ecological fitness of suitors advertising superior somatic structures (e.g., ornaments and weapons), motility competence (e.g., courtship dances), social aptitude (e.g., conflict mediation and instigation), and/or other survival characteristics also promotes the vertical and, where applicable, horizontal spread of beneficial inherited traits, such as tolerance to stressors and toxins (Lujan et al, 2007), pathogen virulence (Gibson, 2001; Chandler et al, 2005; Nielsen and Heitman, 2007), biofilm formation (Ghigo, 2001), and cell aggregation (Hirt et al, 2002; Butler et al, 2009), within subdivided populations at greater rates and efficiencies (Clark, 2011a, 2012a, 2013). Although microbial mate selection appreciably favors virulence and transmission of infectious diseases, major evolutionary transitions, and emergence of primitive social intelligences (Clark, 2012a, 2013), the biological and computational processes used by microbes to identify and correct performance faults during mate selection remain, with few exceptions, poorly understood (Ricci, 1990; Clark, 2010a,b,c,d; Phadke et al, 2012). …”