Ribosomal RNA-encoding DNA introgression across a narrow hybrid zone between two subspecies of grasshopper

Abstract

A ribosomal RNA-encoding DNA (rDNA) cloned sequence, consisting of a 0.8-kilobase fragment from the 26S/nontranscribed spacer region, was used to identify diagnostic restriction enzyme fragments that distinguish the Moreton and Torresian subspecies of the grasshopper Caledia captiva. These restriction fragments were then used to study patterns of rDNA variation across a narrow geographical hybrid zone between the two subspecies. The pattern of rDNA variation that emerged after the analysis ofover 250 individuals clearly demonstrates the asymmetrical introgression of the Moreton ribosomal RNA genes into the Torresian subspecies. This asymmetric movement of genetic material occurs even though there exists extreme postmating F2 and backcross inviability between the two subspecies. From our data, as well as those of previous chromosomal and allozymic studies, we are able to support the occurrence of nonrandom processes such as biased gene conversion and/or natural selection. Because the rDNA loci in the Moreton and Torresian individuals are located in different regions on chromosomes 10 and 11, it should be possible to determine the relative contributions of conversion, natural selection, and these sorts of processes to the pattern of introgression of the Moreton rDNA into the Torresian subspecies.How reproductive isolation develops during the speciation process remains a fundamental and unanswered question in evolutionary biology. As a corollary ofthis question, one can inquire about the consequences of repeated hybridization between partially reproductively isolated populations. Grant (1) has stated, in reference to the findings of Anderson (2), that long-term backcrossing of hybrid individuals to the parental types can result in ".... convergences between previously separate phyletic lines ...." However, it is also apparent that the introduction, maintenance, and persistence of foreign genetic material, despite significant pre-and/or postmating isolation, must be mediated by factors such as genetic drift, migration, and/or natural selection. Thus, the definition of interacting processes that lead to introgression (2) of genetic material is of fundamental importance in understanding how genetic systems may be perturbed. Indeed, it has been advocated that a major stimulus to speciation involves hybridization (3). Furthermore, the quantitation of the effects of factors such as genetic drift, migration, and selection is equally fundamental in understanding the evolution of organisms.In order to examine the above parameters, it is necessary to identify hybridizing taxa that have the following characteristics: (i) significant levels of reproductive isolation; (ii) morphological, physiological, or genetic markers that can be used to identify genomic components in parental and hybrid individuals; and (iii) definable differences in the habitats occupied by the taxa. Such a system has been identified in the grasshopper Caledia captiva. In particular, two subspecies (Moreton and Torresian) of C. captiva meet and f...

Gene flow across a chromosomal tension zone. I. Relicts of ancient hybridization

“…In addition to the 29 and 21 fragments, a "32" kb variant has been reported in a Torresian population located approximately 1200 km from the contact zone (Arnold et a!., 1987a). In the present analysis we have detected four variants; these are the 21, 27, 29 and the 32 fragments As stated previously, there were two additional rDNA RFLPs (2.7 and 3.2) that have been assayed in the present analysis.…”

“…RFLPs that are diagnostic for the Torresian and Moreton rDNA and mtDNA have been previously identified (Arnold et a!., 1987a;Marchant, 1988). Cla I restriction digestion of total DNA followed by gel electrophoresis, transfer of the restricted DNA to Gene Screen (New England Nuclear) and hybridization to a 32P nick-translated 08 kb rDNA sequence (Arnold et al, 1987a) were used to resolve the rDNA markers. The restriction endonucleases Msp I, Hae III, Hind III and Xba I were used to assay for mtDNA markers (as described Figure 1 Populations sampled for rDNA, mtDNA and/or allozyme frequency (see Table 1 for population designations).…”

“…No introgression of Moreton chromosomes has ever been detected outside the narrow zone of hybridization (Shaw et a!., 1987), but Moreton rDNA, mtDNA and allozyme markers are present in some Torresian populations (Arnold et a!., 1987a;Marchant 1987Marchant , 1988Marchant et a!., in preparation).…”

“…The effect of the centromere position differences has been estimated to account for 46 per cent of the inviability of Torresian/Moreton F2 hybrids; Coates and Shaw (1984) suggested that the remaining hybrid breakdown may be associated with "genic" differences between the taxa. Previously, allozyme differences Daly eta!., 1981), restriction-fragment length polymorphisms (RFLPs) of the ribosomal DNA (rDNA) (Arnold et a!., 1987a) and mitochondrial DNA (mtDNA) (Marchant, 1988), and variation in the cytological distribution and associated DNA sequences of heterochromatin (Shaw et a!., 1976;Arnold and Shaw, 1985;Arnold, 1986) which distinguish Torresian from Moreton, have been described. The distributions of these markers along transects taken across the hybrid zone have been studied (Moran, 1979;Shaw et a!., 1979;Arnold et a!., 1987a;Marchant et a!., in preparation;Moran and Shaw, 1977).…”

“…Previously, allozyme differences Daly eta!., 1981), restriction-fragment length polymorphisms (RFLPs) of the ribosomal DNA (rDNA) (Arnold et a!., 1987a) and mitochondrial DNA (mtDNA) (Marchant, 1988), and variation in the cytological distribution and associated DNA sequences of heterochromatin (Shaw et a!., 1976;Arnold and Shaw, 1985;Arnold, 1986) which distinguish Torresian from Moreton, have been described. The distributions of these markers along transects taken across the hybrid zone have been studied (Moran, 1979;Shaw et a!., 1979;Arnold et a!., 1987a;Marchant et a!., in preparation;Moran and Shaw, 1977). These analyses have found that the geographical change-over from insects having Torresian allozyme, rDNA and mtDNA markers, to those having Moreton markers, corresponds nearly to the null points shown by the frequencies of the chromosome structural markers (Shaw et a!., 1979;Shaw eta!., 1985).…”