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Factors Determining the Frequency of the Killer Trait Within Populations of the Paramecium Aurelia Complex

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Factors Determining the Frequency of the Killer Trait Within Populations of the Paramecium Aurelia Complex Copyright 0 1987 by the Genetics Society of America Factors Determining the Frequency of the Killer Trait Within Populations of the Paramecium aurelia Complex Wayne G. Landis Environmental Toxicology Branch, Toxicology Division, Chemical Research and Development Center, Aberdeen Proving Ground, Maryland, 21010-5423 Manuscript received March 3, 1986 Revised copy accepted September 15, 1986 ABSTRACT The factors maintaining the cytoplasmically inherited killer trait in populations of Paramecium tetraurelia and Paramecium biaurelia were examined using, in part, computer simulation. Frequency of the K and k alleles, infection and loss of the endosymbionts,recombination during conjugation and autogamy, cytoplasmic exchange and natural selection were incorporated in a model. Infection during cytoplasmic exchange at conjugation and natural selection were factors that would increase the proportion of killers in a population. Conversely, k alleles reduced the proportion of killers in a population,acting through conjugation and autogamy. Field studies indicate that the odd mating type is prevalent in P. tetraurelia isolated from nature. Conjugation and therefore transmission by cyto- plasmic transfer would be rare. Competition studies indicate a strong selective disadvantage for sensitives at concentrationsfound in nature. Natural selection must therefore be the factor maintaining the killer trait in P. tetraurelia. YTOPLASMIC inheritance is a widespread phe- The two hosts, P. tetraurelia and P. biaurelia, are C nomenon that includes sex and drug resistance sibling species within the P. aurelia complex as con- in bacteria, CO2 sensitivity in Drosophilia melanogaster structed by SONNEBORN(1975). Paramecia of this and possibly certain tumors in mammals. Indeed, the complex undergo two major sexual processes, conju- origin of the eukaryotic cell may have been dependent gation and autogamy. Conjugation occurs when re- on certain chloroplast and mitochondria-like inclu- active cells of one mating type are mixed with those sions similar to the bacterial endosymbionts found in of the complimentary mating type, resulting in first many present-day organisms. GILL and HAIRSTON cell clumping and then pairing. Paramecia undergoing (1972) have proposed that bacterial symbionts may conjugation do not feed and thereby do not take up mediate protozoan community structure. Fertility the toxin produced by the killers. Sensitives are there- barriers among mosquito species of the genus Culex fore protected and can mate with killers. The two are caused by a symbiotic rickettsia (YEN and BARR micronuclei undergo meiosis and the macronucleus 1973). However, little attention has been paid to the breaks down. Haploid nuclei are exchanged, fertiliza- factors affecting the inheritance of cytoplasmically tion occurs and new macronuclei and micronuclei inherited traits at the population level. develop, restoring the normal vegetative state. During The killer trait, a classic case of cytoplasmic inher- conjugation, a cytoplasmic bridge may form, enabling itance, observed within Paramecium biaurelia and P. the cytoplasm of the two partners to mix. Autogamy tetraurelia is caused by the bacterial endosymbionts of is a form of self-fertilization rendering the individual the genus Caedobacter, commonly called kappa homozygous at all loci. It occurs at intervals in lines if (PREER, PREER andJuRAND 1974). Paramecia contain- starved paramecia are not allowed to mate. The proc- ing the endosymbiont (killers) release a toxin that ess requires a fission to restore the normal nuclear causes the death of paramecia not maintaining the complement. For a detailed account of conjugation same bacteria (sensitives). Sensitives incur symptoms and autogamy, see SONNEBORN(1943, 1974) and specific to the type of endosymbiont involved. The BEALE(1954). presence of kappa within a paramecium depends on Although the killer trait was among the earliest the KK or Kk genotype of the host. When an organism cases of cytoplasmic inheritance discovered and has becomes kk, the kappa are lost (SONNEBORN1943). S been extensively studied by PREER,SONNEBORN and alleles at loci SI and Sz, discovered within stock 29 of others, its population genetics, ecological and evolu- P. tetraurelia, increase the probability of kappa loss tionary significance largely have been ignored. GILL (BALBINDER1959, 1961). The distribution of kappa (1972; GILL and HAIRSTON1972) has hypothesized is worldwide, with stocks originating from North that the superior competitive ability of P. biaurelia America, Central America, Europe, Japan and Aus- compared to P. triaurelia and P. pentaurelia within a tralia (PREER,PREER and JURAND 1974). seep near Ann Arbor, Michigan, may be due to an Genetics 115: 197-205 (January, 1987) 198 W. G. Landis unidentified killer endosymbiont. GILLand HAIRSTON TABLE I further surmise that endosymbionts may play an im- The changes of the proportions of the five classes of paramecia portant role in protozoan community structure. in a mixed population of killers and sensitives This report describes the current revision of the model used during the field and laboratory studies of Class a b X Y I LANDIS(1981, 1986) on the role and evolution of the ~ ~~ KK, KK,no Kk, Kk,no M,no killer trait in natural populations of paramecia. As the Genotype kappa kappa kappa kappa kappa ~ fieldwork began in the mid 1970s, earlier versions of Proportion of each class A B X Y z this model posed certain important questions as to in the population at mating-type frequency, the effectiveness of the killer generation n trait at low densities of paramecia, and the roles of Relative number of each A’ B’ X’ Y’ Z’ conjugation and autogamy in the evolutionary strat- class in the population egy of paramecium. The importance of the model, as after natural selection, with most models of this genure, is its interaction and infection and loss have occurred influence upon the formation of theories and the precise design of experiments to test the predictions If no sexual process occurs, then the proportion of the classes in the next generation after natural selection, in- of the theory. fection and loss have taken place will be represented by Af Bf Xf Yf Zf THE MODEL If conjugation takes place, the proportions of A,, Bf, etc., will be affected by recombination and cytoplasmic ex- Within a population of killers and sensitives of the change. The resulting proportions are same species there are five possible classes of individ- A, B, X, Y, Z, uals in regard to genotype and cytoplasmic characters, Since not all the members of the population will undergo ignoring the SI and S2 loci. These classes, along with each of the above processes during the same generation, most of the symbols used in this paper, are listed in the fraction that undergoes only a fission will be 7,conju- Table 1. Class a is homozygous K and contains kappa. gation, /3, and for autogamy, a. When properly manipu- It is killer. Class b is like class a, but lacks kappa and lated, the resulting proportions of the five classes can be is therefore sensitive. Classes x and y are like a and b, calculated. The proportions will be in generation n+ 1: respectively, but are heterozygous. Class z is KK, lacks An+, &+I &+I Y~+I Zn+1 kappa and is sensitive. The proportions within popu- lation of the five classes at generation, n, are desig- nated A, B, X, Y and Z. As explained below, these at each locus on the order of 1 or 2% (LEWONTIN proportions will be determined by the relative Dar- 1974). Therefore, the intents of this model are satis- winian fitnesses of sensitives and killers, the rate of fied by letting Ws remain constant within a range of spontaneous loss of kappa from the cytoplasm (L),the 0.95 to 1.0 times that of Wk. rate of infection of the endosymbiont from ingestion The spontaneous loss of kappa, occurring at rate L (C), cytoplasmic exchange (R)and the relative pro- each generation, will reduce the proportions of the portions of the nuclear genotypes produced at conju- kappa-bearing classes, adding individuals to the sen- gation and autogamy. sitive classes. Loss often occurs in the laboratory and The Darwinian relative fitness component, w,ex- may be due to a number of causes. The host outgrow- presses the effect of natural selection upon the various ing the endosymbiont, certain temperature regimes, phenotypes. The assumptions and validity of various antibiotics and other causes are known to eliminate selection models have been extensively discussed kappa from genetically competent hosts. (DOBZHANSKY1970; CROWand KIMURA 1970; WAL- Infection may occur in two ways. First, infection LACE 1968) and will not be mentioned here. Assuming may result from the ingestion of the infectious kappa that the only factors modifying the relative fitnesses particles by a competent host. However, in the labo- of the five classes are the effects of the presence or ratory such infection has been difficult to accomplish, absence of kappa, the sensitive classes can be assigned requiring a high density of kappa and competent the fitness W,, the killer W,. The relative fitness of sensitives in the presence of Ca+ and Mg’ ions (MUEL- both groups is frequency- and density-dependent, with LER 1963, 1964). In view of the conditions required, the fitness of the sensitive classes approaching zero the rate of infection due to ingestion, C, is thought to under conditions usually found in the laboratory. be low in nature. However, populations in nature seem very unlikely to The other parameter of infection is the rate of produce the enormous densities used in routine labo- infection (transmission) due to cytoplasmic exchange, ratory killing tests. Furthermore, very large differ- R. Cytoplasmic exchange may occur when a killer ences in fitnesses in nature are extremely rare, varying mates with a sensitive that is genetically competent Killer Paramecia 199 following the conjugation. R is a function of the rate TABLE 2 of cytoplasmic exchange and the probability of an Equations describing the inheritance of the killer trait in infectious particle invading and multiplying within a populations of paramecia competent host.
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