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Maintenance of a “Parasitic” B Chromosome in the Grasshopper Melanoplus Femur-Rubrum

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Maintenance of a “Parasitic” B Chromosome in the Grasshopper Melanoplus Femur-Rubrum MAINTENANCE OF A “PARASITIC” B CHROMOSOME IN THE GRASSHOPPER MELANOPLUS FEMUR-RUBRUM UZI NUR Departmant of Biology, Uniuersity of Rochester, Rochester, New York 14627 Manuscript received April 20, 1977 Revised copy received August 1, 1977 ABSTRACT About 10-15% of the males and females of the grasshopper Melanoplus femur-rubrum collected near Rochester, New York, possessed a supernumerary B chromosome. The frequency of the B chromosome remained fairly constant during the years 1971-1974. The B chromosome was shown previously to be transmitted at a rate of about 0.5 and 0.8 by 1B males and females, respec- tively. This study was designed to determine the forces preventing the B chromosome from increasing in frequency due to the high rate of transmission by the females. Eighty inseminated females collected in the wild were analyzed cytologically together with their embryos (10-20 per female). Ten of the 80 females had a B chromosome, and they transmitted it at a rate of about 0.75. Among the 983 embryos analyzed, 0.141 had one B, 0.007 had two, and the mean number of B chromosomes per embryo was 0.155. The frequency of the B chromosome in the sperm pool (0.061) was consistent with a 0.5 rate of transmission. Individuals with two B chromosomes apparently have low viabil- ity, because about six were expected, but none was found among 851 adult males and females examined. The data suggest that the viability of the 1B individuals was only about 0.86 that of the OB individuals. There was no evi- dence that the B chromosome increased the fecundity of either the 1B males or females. It was concluded, therefore, that the B chromosome reduced the fitness of all the individuals carrying it and was thus “parasitic,” and that it was maintained in the population only because of its high transmission rate. The maintenance of other B chromosomes with high transmission rates is reviewed. chromosomes (supernumerary chromosomes) are present in some of the indi- Bviduals of a population, but not in others, are not homologous to the regular chromosomes, and usually have little effect on the phenotype. B chromosomes are present in many animal and plant species (WHITE1973; JONES1975). Some of the B chromosomes are mitotically unstable (NUR1963,1969a; WHITE1973) or undergo nondisjunction during meiosis (JONES1975), and in some species these unusual types of behavior may serve as accumulation mechanisms that, like meiotic drive, would tend to cause the frequency of the B chromosomes to increase from generation to generation. In several species that possessed an accumulation mechanism, the frequency of the B chromosomes remained stable over several generations or years (NUR196910; HEWITT1973b), and this stability could result only from selection against some of the individuals with B chromo- Genetics 87: 499-512 November. 1977. 500 U. NUR somes. The selection against them may take place in two ways, which were termed by WHITE(1973) the “heterotic” and “parasitic” models. According to the former model, the fitness of individuals with one B chromosome (1B individ- uals) is higher while that of those with higher numbers of B chromosomes is lower than OB individuals. According to the “parasitic” model, the mean fitness of all the classes of individuals with B chromosomes is lower than that of OB individuals. More complex models in which, for example, the B chromosomes are “heterotic” in one sex but “parasitic” in the other are possible. It is also possible that different models may apply to the same B chromosome in different popula- tions, to B chromosomes of different species, or to different B chromosomes of the same species. It has been pointed out earlier (NUR1969a; Lucov and NUR 1973) that in species like the grasshopper Melanoplus femur-rubrum in which the frequency of B chromosomes is fairly low (0.10-0.15) and the tendency to accumulate is fairly high (the combined rates of transmission in both sexes is 1.2-1.3), the B chromosome cannot be “heterotic” in both sexes, because even if 2B individuals were effectively lethal, their death would not remove enough B chromosomes to offset the tendency to accumulate. The possibility could not be ruled out, how- ever, that in such species the B chromosome was “heterotic” in one sex but “para- sitic” in the other. The aim of this study was, thus, to try to obtain information about the fitness of OB, 1B and 2B males and females of Melanoplus femur- rubrunz in order to determine whether in this species the B chromosome is main- tained according to the “heterotic,” the “parasitic,” or a more complex model. MATERIALS AND METHODS The males and females analyzed were collected in a field and an adjacent lawn near the Whipple Park housing project of the University of Rochester, Rochester, New York. The 1971, 1972, and 1973 collections were made from the same area, which was about 30 x 120m. In 1974, part of the field was plowed and this part and the adjacent lawn had very few grasshoppers. Thus, the collection was restricted to an area of about 30 x 30 m, which comprised the southwest section of the area from which previous collections were made. In 1973, adult males were collected during September and the first week of October. Sixty- eight adult females were collected on September 12, 1973, and placed individually in small cardboard cages with lettuce, oat bran and damp sand. In the next six days six females died and 32 laid one egg pod each. Because of the possibility that additional mortality might invali- date the sample, all the females were killed and fixed. A second group of 79 females was collected on September 25, 1973, and maintained as before. Only three females died during the next 16 days, at which time 51 of the females had oviposited, and these were fixed for analysis as soon as laying was detected. The nonlaying females were all fixed on the 16th day after their collection. Most of the eggs of two of the 83 laying females did not contain embryos. The eggs of one female were assumed to have developed parthenogenetically because all the embryos were very small, relative to those which were laid on the same day by other females, and some of the embryos contained haploid cells. Thus, the eggs of those three females were not included in the analysis. The eggs of the remaining 80 females were allowed to develop for 10-14 days and the embryos were then dissected out, treated with a hypotonic solution con- taining colchicine (Lucov and NUR1973) and then fixed. The laying females were examined cytologically prior to the dissection and the fixation of their embryos. When a female was four,d to possess a B chromosome, about 20 of her embryos “PARASITIC” B CHROMOSOME 501 were treated and fixed. For the OB females, either 10 or about 20 embryos were treated and fixed, depending on the time available that day. In 1974, immature and adult males and imma- ture females were collected between August 23 and September 16. The adult males were fixed immediately. The immature males and females were kept in the laboratory until they became adults, during which time a few died. The rest were then fixed and analyzed cytologically. RESULTS The apperrrance and behavior of the B chromosome The B chromosome was about the size of several of the medium-sized regular chromosomes. Unlike all the regular chromosomes, however, it was metacentric, and as such could be readily identified during mitosis (Figures 1 and 2). In 1B males, during prophase I of meiosis, the B and the X chromosome both ap- peared positively heteropycnotic (heterochromatic), but the B was slightly shorter than the X chromosome (Figure 3). The B chromosome moved to one FIGURE1.-Mitosis in a female embryo with one metacentric B chromosome (lower center) and 24 regular chromosomes. FIGURE2.--Mitosis in a male embryo with two metacentric B chromosomes and 23 regular chromosomes. FIGURE3.-Diplotene-diakinesis in a spermatocyte with one heterochromatic B chromosome (lower right). The heterochromatic X chromosome is at the lower left. FIGURE4.-Diplotene-diakinesis in a spermatocyte with two small heterochromatic BT chromosomes. One BT chromosome is near the X chromosome and the other is slightly above it. 502 U. NUR of the poles in anaphase I and divided regularly during anaphase 11. The B chromosome was mitotically stable, and there was no evidence to suggest that it tended to be lost at any time between the zygote and the spermatids. As has been reported by Lucov and NUR(1973) , during anaphase I of oogenesis the B chro- mosome tended to move preferentially into the secondary oocyte, rather than into polar body I, and this tendency apparently caused it to be transmitted at a rate which was significantly higher than the expected rate of 0.5. The frequency of the B chromosome among adults The results of the €our years of sampling the Whipple Park population are presented in Table 1. The frequency of the B chromosome among both sexes ranged from 0.107 to 0.136. In three of the four years, its frequency among females was lower than among males, but none of the differences was statisti- cally significant. The frequency of the B chromosome in 1971 (0.107) was somewhat lower than in the subsequent years, but at least for the years 1972- 1974 its frequency remained fairly constant. One unexpected result of the sampling was the increase in the frequency of a small extra chromosome from 1971-1973 to 1974. In its behavior in males, this chromosome appeared to be similar to a small B chromosome described previously by STEPHENSand BREGMAN(1972) and designated by them BT.
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