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Effects of Polymorphic Robertsonian Rearrangements on the Frequency Eur. J. Entomol. 104: 653–659, 2007 http://www.eje.cz/scripts/viewabstract.php?abstract=1271 ISSN 1210-5759 Effects of polymorphic Robertsonian rearrangements on the frequency and distribution of chiasmata in the water-hyacinth grasshopper, Cornops aquaticum (Orthoptera: Acrididae) PABLO C. COLOMBO* Laboratorio de Genética, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, (1428) Ciudad Universitaria, Buenos Aires, Argentina; e-mail: [email protected] Key words. Acrididae, Cornops aquaticum, Robertsonian polymorphisms, recombination, chiasma interference, chiasma distribution Abstract. The New World grasshopper Cornops aquaticum (Leptysminae: Acrididae) shows a geographical pattern for three Robert- sonian polymorphisms in its southernmost area of distribution in Argentina and Uruguay. The frequency and distribution of chias- mata were analysed in five Argentinian populations. This study reveals a strong redistribution of chiasmata in fusion carriers, with a reduction in proximal and increase of distal chiasma frequency in fusion bivalents and trivalents, when all three karyotypes were compared. However, when only fusion bivalents and trivalents were compared, chiasma frequency was significantly higher in the former than in the latter. This higher chiasma frequency in fusion bivalents is due to an increase in proximal chiasma frequency. It is argued that the reduction in proximal chiasma frequency (relative to unfused bivalents) in fusion bivalents may be due to interfer- ence across the centromere. Proximal chiasma reduction in trivalents may be attributed either to a physical effect of structural hetero- zygosity or to an adaptation to the polymorphic condition. Therefore the differences in the distribution of chiasmata in trivalents and Robertsonian bivalents have different causes. INTRODUCTION same length and low chiasma frequency are preadapted to Robertsonian rearrangements, as well as inversions and undergo a Robertsonian change that might lead to a poly- whole-arm reciprocal translocations (WARTs), are chro- morphism, especially if chiasmata are localized distally mosome rearrangements that may cause a reduction in (Bidau & Mirol, 1988). However, in some cases the Rob- fertility in structural heterozygotes due to meiotic irregu- ertsonian change leads to a reduction in chiasma fre- larities, although to a lesser extent than interchanges quency and distal localization of chiasmata in the (Hewitt, 1979). As a matter of fact, heterozygotes for rearranged chromosomes, amidst chromosomes on which chromosomal rearrangements are less fertile than both the frequency and distribution of chiasmata are unre- homozygotes; as a consequence the heterozygotes are less stricted (Colombo, 1993; Bidau, 1990). fit. In this case (subdominance for fitness) selection In the present paper we examine chiasma position and against heterozygotes leads to the loss of the least fre- frequency in the water-hyacinth grasshopper, Cornops quent karyomorph (Hedrick, 1983). Therefore, the rear- aquaticum Bruner (Leptysminae: Acrididae). This New rangements would not be expected to be seen in a World grasshopper is semi-aquatic and inhabits water- polymorphic state. However, all the mentioned rearrange- hyacinth, Eichhornia crassipes, upon which it feeds and ments are seen sometimes in polymorphic state as com- oviposits (Adis & Junk, 2003). Early in the 20th century pensatory mechanisms arise that suppress the meiotic the blue-flowered water-hyacinth E. crassipes was intro- irregularities in heterozygotes (e.g., non homologous duced to other continents (mainly Africa) as an orna- pairing of mutually inverted sequences of inversion het- mental plant. Free of natural enemies, it has become the erozygotes in Trimerotropines and other grasshoppers “World’s Worst Water Weed”, choking dams, covering with pericentric inversions (Colombo & Confalonieri, lakes and rivers and barring people from free access to 1996), or proximal chiasma suppression in Robertsonian water (Centre et al., 2002). Biological control using wee- polymorphisms (Bidau, 1990; Colombo, 1990). In the vils that feed on water-hyacinth has so far been unsuc- case of Robertsonian translocations the most frequent cessful (Albright et al., 2004). Therefore, C. aquaticum is irregularity in heterozygotes consists of linear orientation considered to be a possible biological control agent, and in metaphase I, leading to imbalanced gametes. This is is being widely studied, especially from an ecological most frequent in Robertsonian sub-metacentrics with point of view. Currently, it is being considered for pos- highly unequal arm length and high chiasma frequency sible release in South Africa (Oberholzer & Hill, 2001). It (Baker & Bickham, 1986; Bidau, 1991; Searle, 1993). has a wide distribution (from 23°N to 35°S on the This means that acro-telocentric pairs with roughly the American Continent) (Lhano et al., 2005); in the south- ernmost part of its distribution a complex system of three * Affiliated to CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas). 653 Fig. 1. Metaphase I plates showing chiasma position in different karyotypes of Cornops aquaticum. A. Standard karyotype (no centric fusions), all chromosomes acro/telocentric. Notice the abundance of proximal chiasmata. Arrow: supernumerary segment in the smallest bivalent of the complement. B. Homozygote for one centric fusion and heterozygote for two other fusions. C. Another metaphase I plate from individual B. D. Individual homozygote for all three centric fusions. P – proximal; I – intersitial; D – distal chiasma. Solid arrowhead: Robertsonian trivalent. Outline arrowhead: Robertsonian (meta/submetacentric) bivalent. Bars: 10 mm. Robertsonian polymorphisms occurs, with the consequent Although arguably diplotene cells are preferable for chiasma loss of recombination (P.C. Colombo, in prep.); in the rest scoring, due to the chromosome condensation at metaphase I, it of South-America it seems to be free of chromosomal should be pointed out that diplotene cells are rare in this mate- polymorphisms. In the present paper, the redistribution of rial, whereas metaphase I cells are abundant, which allows larger samples. Furthermore, it is extremely difficult to see chiasmata triggered by rearrangements is described and where the centromere lies in diplotene cells, thus rendering it interpreted. This redistribution is found both in Robert- impossible to distinguish between proximal and distal sonian homozygotes and heterozygotes – but here these chiasmata. This is especially true of submetacentrics; and last, are presented as two different cases. Chiasma redistribu- unlike other material, metaphase I in grasshoppers is a favour- tion in heterozygotes is caused either by a direct effect of able stage for separating chiasmata into proximal, interstitial, the fusion on synapsis or adaptation to the polymorphic and distal (Fig. 1). Chiasma frequencies were recorded as condition. In contrast, chiasma redistribution in Robert- proximal (P), interstitial (I) or distal (D) to the centromere, since sonian homozygotes is produced by interference acting there is no need for a more precise chiasma distribution data. across the centromere. In this paper, we test these Alternative ways of more precisely recording chiasma distribu- hypotheses in order to shed light on this problem. tion (such as the “chiasma graph” method, Wada & Imai, 1995; Imai et al., 1999) may be used in the future, but at this stage of MATERIAL AND METHODS the research the precision afforded by the method employed in this paper is accurate enough for our purposes. In this study, five Argentinian populations were sampled and Chiasma frequency and distribution was studied in three analysed cytologically. These populations, from north to south, groups of chromosomes: (a) acro-telocentric bivalents of are: Corrientes (20 males), Rosario (8 males), San Pedro (12 unfused homozygotes; (b) trivalents of heterozygotes; (c) meta- males), Zárate (24 males), and Tigre (14 males). Testes were submetacentric bivalents of fused homozygotes. Chiasmata were dissected and fixed in 3 ethanol: 1 acetic acid. The cytological classed as proximal (P), interstitial (I) or distal (D) with respect analysis was performed by squashing some follicles in propri- to the centromere (Table 1). onic haematoxylin. Male meiosis was studied; chiasmata were With the exception of the three small pairs (9, 10, and 11), registered on 10 metaphase I plates per individual and classified which do not take part in the fusions and have generally one as proximal, interstitial or distal with respect to the centromere. distal chiasma, the eight acro-telocentric chromosome pairs 654 TABLE 1. Chiasma frequency and distribution in acrocentric bivalents, trivalents and fusion metacentrics. P, I, D, and T – proximal, interstitial, dis- tal, and total chiasmata per acrocentric bivalent, respectively. PII , III, DII , and TII – id. per metacentric bivalent. PIII , IIII , DIII , and TIII – id. per trivalent. N – number of bivalents involved in centric fusions per individuals. The specimens were from Corrientes (C), Zárate (Z), San Pedro (SP), Rosario (R ) or Tigre (T). Individual N PII III DII TII PIII IIII DIII TIII P I D T Z05002 3 – – – – 0.2 0.3 1.73 2.23 0.15 0.4 0.45 1.0 Z05004 3 – – – – 0.2 0.3 1.6 2.1 0.7 0.15 0.15 1.0 Z05028 2 0.9 0.1 1.8 2.8 0.2 0.4 1.5 2.1 0.77 0.17 0.3 1.23 Z05026 3 1.16 0.33 1.0 2.5 1.16 0.5 1.66 2.33 0.92 0 0.08 1 Z05012
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