Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species

Abstract

Mitotic chromosomes of the European water frogs Rana ridibunda and Rana lessonae, the parental species of Rana esculenta, differ significantly in their centromeric regions: when C-banded or when made fluorescent, the centromeres of R. ridibunda (and of ridibunda chromosomes in R. esculenta) are visible as a conspicuous dark granule or as a conspicuous fluorescent spot; the centromeres of R. lessonae (and of the lessonae chromosomes in R. esculenta) are inconspicuous or not fluorescent. Lampbrush chromosomes of these three taxa are described in detail for the first time; those of R. ridibunda and R. lessonae differ significantly in morphostructural characters such as conspicuousness of centromeres and number, form, and location of giant loops as well as in chiasma frequency. Chromosomes of the two parental species can thus be distinguished when present in lampbrush complements of hybrids. Reproduction in both sexes of natural R. esculenta lineages is hemiclonal: only the unrecombined genome of one parental species, usually R. ridibunda, is transmitted to haploid gametes (hybridogenesis). In 18 hybrids from natural populations of Poland, somatic tissues had allodiploid complements with chromosomes from each parental species. In contrast, spermatocytes I of five males and oocytes I of seven of eight females (221 of 222 oocytes) were autodiploid and contained only R. ridibunda chromosomes that formed n bivalents. These 12 hybrids thus were hybridogenetic. A single female hybrid had oocytes I (33 of 34) with genomes of both parental species; they showed various disturbances including tetraploidy, reduced number of chiasmata, and incomplete synapsis resulting in univalents. This individual thus was not hybridogenetic. The irregular lampbrush patterns indicate that such hybrids will have severely reduced fertility and most of their successful gametes will result in allotriploid progeny.

Gametogenesis of intergroup hybrids of hemiclonal frogs

“…Like other non-hybridogenetic hybrids between Rana ridibunda and Rana lessonae (Hotz et al, 1985;Bucci et al, 1990), it evidenced a disturbed gametogenesis caused by the combination of the two heterospecific genomes. The observed approximately triploid spermatogonial metaphases, for example, probably reflect endoreduplication of the L genome without prior elimination of the R genome.…”

“…Hybrids between Rana ridibunda and Rana lessonae, for example, are sterile when the R genome stems from southern parts of the Rana ridibunda range (Hotz et al, 1985 ;Berger et al, 1994 b;unpublished data). Such non-hybridogenetic hybrids show incomplete pairings between the Rana ridibunda and Rana lessonae genomes in meiosis I, which probably lead to aneuploid gametes and thus render the individuals sterile (Hotz et al, 1985;Bucci et al, 1990). The non-hybridogenetic offspring of cross 02.43 is an example of such hybrids.…”

“…(ii) Cytological procedures and fluorescence in situ hybridization (FISH) Mitotic and meiotic chromosomes from intestinal tissue and/or testis were prepared as previously described (Bucci et al, 1990). Mitotic and meiotic preparations were banded using Arrighi & Hsu's (1971) method for staining of heterochromatin.…”

Isolation and expression ofRlYB2, a germ cell‐specificY‐boxgene inRana

“…The development of the germ cells in green frogs of the genus Rana has been thoroughly investigated by means of cytological, genetic and cytogenetic approaches (Uzzell et al 1980;Bucci et al 1990Bucci et al , 1999Ragghianti et al 1995;Ogielska & Kotusz 2004). Interesting information emerged from studies about Rana esculenta gametogenesis (Chieffi et al 2000;Ferrara et al 2004;Meccariello et al 2004).…”

“…The hybrid condition is recovered at the next generation by backcrossing with the parental species whose genome was eliminated (Tunner & Heppich-Tunner 1991). In spite of the molecular mechanisms of hybridogenesis is still unknown, cytogenetic studies and morphological inspections demonstrated the presence of alterations in the gametogenesis of the hybridogenetic frogs (Bucci et al 1990;Ogielska 1990). In addition, a delay in sexual maturation was observed in R. esculenta when compared to the parental species .…”