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Generating High Variability of B Chromosomes in Eyprepocnemis Plorans (Grasshopper)

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Generating High Variability of B Chromosomes in Eyprepocnemis Plorans (Grasshopper) Heredity 71 (1993) 352—362 Received 5 January 1993 Genetical Society of Great Britain Generating high variability of B chromosomes in Eyprepocnemis plorans (grasshopper) M. D. LOPEZ-LEON, J. CABRERO, M. C. PARDO, E. VISERAS, J. P. M. CAMACHO* & J. L. SANTOSI Departamento de Genética, Facu/tad de Ciencias, Un/versidad de Granada, E- 18071 Granada, Spa/n and tDepartamento de Genét/ca, Facultad de B/o/ogIa, Un/vers/dad Comp/utense de Madrid, E-28040 Madrid, Spa/n Twenty-eightprogeny analyses (PAs) performed on specimens of E. plorans collected from four natural Iberian populations have been informative about the transmission of rare B chromosome types or the de novo origin of some of them. At least ii rare B-types have been found in addition to the predominant ones: B1 in Daimuz, B2 in Jete and Salobreña, and B5 in Fuengirola. The presence in two controlled crosses of one embryo carrying a B-type which was absent in the parents suggests that these B variants (B20 and B )haveoriginated de novo. Eleven other PAs suggest that new B derivatives are recurrently arising in these populations. The most frequent B chromosome mutation was centromere misdivision that originated four different B-types (B2m1,B110,B210 and Bmjnj). Other rearrangements were pericentric inversions (B211, B212 and B213), inverse tandem fusion (B211), centric fusion (B11) and deletions (B2d1andB2d2).Thefour B derivatives produced by centromeric misdivision are significantly eliminated during sexual transmission, most probably owing to deficiencies in the control of chromosome movement by their hemicentromeres. Those derived from translocations showed Mendelian transmission but deletion B variants showed a tendency to elimination. Our results suggest that B chromosome substitution of B1 by B2 in the Salobreña and Jete populations could be achieved by differences in relative transmission efficiency, as in one controlled cross, where the female carried 1 B1 plus 1 B2, B2 was significantly overtransmitted and B1 eliminated. Keywords:Bchromosomes, coevolution, drive, genomic parasitism. Introduction Arana, 1990) although three types are prevalent: B1, B2 and B5. B1 is the most frequent in all the populations Bchromosomes constitute one of the most intriguing of the eastern (from Tarragona to AlmerIa) and west- polymorphisms present in a large number of natural ern zones (Cádiz and Huelva) of distribution, and for populations of plant and animal species (Jones & Rees, this reason it has been considered the original B in the 1982). Some properties of Bs have been investigated, Iberian Peninsula (Henriques-Gil et al., 1984). B2 is the mainly from the cytological point of view, although main type in the province of Granada and eastern questions about their origin and their maintenance in Málaga, and B5 is restricted to western Málaga. natural populations remain largely unsolved. The evolution of Bs implies their origin from the One of the most striking B chromosome poly- chromosomes of the standard complement and subse- morphisms described to date is that shown by the quent differentiation to their present form. Further- grasshopper Eyprepocnemis plorans. Bs are present in more, in populations of a given species different but almost all natural populations from the entire geo- related B variants can also be generated and the graphical distribution in the Iberian Peninsula, i.e. the establishment and maintenance of these variants will Mediterranean and Atlantic coastal regions from depend on their transmission and their effects on the Huelva to Tarragona. About 30 different B variants fitness of B-carriers. Most Bs investigated to date show have been distinguished according to different accumulation mechanisms that may be enough to morphology and C-banding patterns (Henriques-Gil & explain their maintenance even though the Bs are detri- mental to carrier fitness (Nur, 1977). The three main *Correspondence. types of Bs of E. plorans constitute an exception to this VARIABILITY OF B CHROMOSOMES 353 general rule as they are transmitted in a Mendelian remaining one, both males were placed simultaneously ratio in populations where they are the most frequent B with the female and the frequency of mating exhibited variant: B1 at Daimuz (Valencia), B2 at Jete and by each male recorded, for which purpose one of the Salobreña (Granada) and B5 at Fuengirola (Malaga). males was marked on the pronotum with nail varnish. The possible causes of maintenance of this widespread The other 20 PAs came from females collected in the polymorphism have been discussed by López-León et field when they were gravid. The effective paternity a!. (1992). The present paper deals with the transmis- displacement existing in E. plorans (López-León et aL, sion rates of rare B variants that have appeared in the 1993)means that gravid females may be considered as populations mentioned above and demonstrates the de controlled crosses because the constitution of the novo origin of some of them and their possibilities of parental male can be inferred from the offspring with a maintenance in subsequent generations. high degree of confidence on the basis of Mendelian transmission exhibited by B1, B2 and B5 chromosomes. Materialsand methods PAs are coded as C (single crosses), DC (double crosses) or 9 (gravid females), followed by the code Specimensof the grasshopper E. plorans were number, the initial of the population (D, J, S or F) and collected at Daimuz (Valencia), Jete and Salobreña the year of sampling. (Granada) and Fuengirola (Málaga). A large number of progeny analyses (PAs) were performed on controlled Results crosses (single or double) and gravid females, from which 28 showed the transmission mode of rare B Figure1 shows the C-banding pattern of all types of Bs chromosome types or else the de novo origin of new B found in the progeny analyses (PAs) performed in this variants. All methods employed in the present investi- work. They are in addition to the standard complement gation are similar to those previously described of 22+ Xci/22 + XX9chromosomes. (Ldpez-León etal., 1991, 1992). The three main Bs show the following charac- Seven progeny analyses were obtained by means of teristics: single (2) or double (5) crosses in which a female was (1) B1 shows two similar sized C-bands on the long mated to one or two males, respectively. Two double arm, the light distal region being conspicuously larger crosses were made by substitution so that they are than the two C-bands as a whole. separated into two independent PAs, one for each (2) B2 in Daimuz also shows two C-bands of similar male, according to Ldpez-Ledn et al. (1991). In the size on the long arm but in the Granada populations S I I $ I B1 82 B B Bj 'L1.1 B1 B, 'IC) B BmBjjj B B B, Fig. I Three main types of B chromosomes in E. plorans: B1 from Daimuz (Valencia), B2 from Daimuz (the first), B2 from Salo- brefla and Jete (Granada) (the second) and B5 from Fuengirola (Málaga) together with 13 other B variants found in these populations. Bmjnj of at least two different sizes were found, which indicates that this is a heterogeneous category. 354 M. D. LOPEZ-LEON ETAL. the interstitial band is larger than the proximal one. (7) B111 is the result of a centric fusion between two B1 The main difference between B2 and B1 is the smaller chromosomes. size of its light distal region. (8) B210 is an isochromosome derived from the B2 by (3) B5 is an acrocentric chromosome similar in size to means of centromere misdivision and subsequent but with a much larger C-band near the centromere chromatid non-disjunction. and smaller light distal region. (9) B2111 is the result of an inverse tandem fusion In addition to these three main types, 12 other between two B2 chromosomes with the loss of the derivatives have appeared in the four populations centromere and the short arm in one of them. sampled. The number of B variants is very high (more Finally, one B variant appeared in Fuengirola than 40, with those described in the present paper) so besides B5 and Bmjnj: B51 which shows the C-banded that it is necessary to codify their names properly in region located at the end of the long arm as a result of order to avoid confusion. We propose that each B an intrachromosomal translocation. variant should be named by the number of the main B from which it is presumed to have been derived, followed by the initial of the chromosomal mutation Inheritanceof rare B chromosome variants from which it arose and an order number. For example, Theresults of all the progeny analyses are shown in B212 means that this B type is derived from the B2 Table 1. Details concerning them are the following. through an inversion and that it is the second B variant risen from this type of rearrangement. B1, B21711 and B,,0. Previous reports (Henriques-Gil et Besides B1 and B2, in Daimuz two other B variants al., 1984; Henriques-Gil & Arana, 1990) indicated appeared: that B1 was apparently absent from the provinces of (1) B110, which is an iso B1 derived from centromere Granada and eastern Málaga. The two populations misdivision and subsequent chromatid non-disjunc- analysed by us in this area (Jete and Salobreña) have tion. This B type was originally described as B12 by shown the presence of this type of B although in a low Henriques-Gil etal. (1984). number of individuals. Thus, seven of our PAs have (2) Bmjnj, which is small, about the size of the short arm permitted the analysis of the mode of inheritance of plus a hemicentromere, and has also arisen through this chromosome in four of which it was transmitted centromere misdivision.
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