Fixation of Deleterious Mutations in Clonal Lineages: Evidence From Hybridogenetic Frogs

Abstract

Abstract. The hemiclonal waterfrog Rana esculenta (RL genotype), a bisexual hybrid between R. ridibunda (RR) and R. lessonae (LL), eliminates the L genome from its germline and clonally transmits the R genome (hybridogenesis). Matings between hybrids produce R. ridibunda offspring, but they generally die at an early larval stage. Mortality may be due to fixed recessive deleterious mutations in the clonally inherited R genomes that were either acquired through the advance of Muller's ratchet or else frozen in these genomes at hemiclone formation. From this hypothesis results a straightforward prediction: Matings between different hemiclones, that is, between R. esculenta possessing different R genomes of independent origin, should produce viable R. ridibunda offspring because it is unlikely that different clonal lineages have become fixed for the same mutations. I tested this prediction by comparing survival and larval performance of tadpoles from within-and between-population crossings using R. esculenta from Seseglio (Se) in southern, Alpnach (Al) in central, and Elliker Auen (El) in northern Switzerland, respectively. Se is isolated from the other populations by the Alps. Enzyme electrophoresis revealed that parents from Se belonged to a single hemiclone that was different from all hemiclones found north of the Alps. Parents from Al also belonged to one hemiclone, but parents from El belonged to three hemiclones, one of which was indistinguishable from the one in Al. Rana esculenta from Se produced inviable tadpoles when crossed with other hybrids of their own population, but when crossed with R. esculenta from Al and El, tadpoles successfully completed metamorphosis, supporting the hypothesis I tested. Within-population crosses from Al were also inviable, but some within-population crosses from El, where three hemiclones were present, produced viable offspring. Only part of the crosses between Al and El were viable, but there was no consistent relationship between hemiclone combination and tadpole survival. When backcrossed with the parental species R. ridibunda, hybrids from all source populations produced viable offspring. Performance of these tadpoles with a sexual and a clonal genome was comparable to that of normal, sexually produced R. ridibunda tadpoles. Thus, in the heterozygous state, the deleterious mutations on the clonal R genomes did not appear to reduce tadpole fitness.

Asexual reproduction: Genetics and evolutionary aspects

“…Finally, in some species, only one half of the genome (maternal or paternal) is retained in the germline without recombination. This phenomenon is called hybridogenesis [63] and has been well documented for the hemiclonal waterfrogs Rana esculenta, in which either the maternal or paternal genome may be retained [64]. In maternal hybridogenesis, male sperm of one parental species is still needed.…”

“…Vol. 64,2007 Review Article produced can stay attached to the mother plant, in which case they can be considered as branches of the same individual. This is different from the production of independent individuals.…”

“…Vol. 64,2007 Review Article 1365 particularity can be used to detect ancient clonality in a group of clonal lineages [82]. To date, this phenomenon has only been found for bdelloids.…”

Effects of geographic distance, sea barriers and habitat on the genetic structure and diversity of all-hybrid water frog populations

“…They thus depend on backcrossing with R. lessonae to form a new generation of hybrids (L-E system). Inter-hybrid matings usually result in RR offspring that are inviable because they are homozygous for recessive deleterious mutations in the clonally transmitted R genome (Vorburger, 2001a). Modifications of this system include reproduction with P. ridibundus instead of P. lessonae in eastern Europe (R-E system), triploid LLR and LRR individuals (can be present in all breeding systems) and the allhybrid populations (E-E system).…”

“…Various studies have shown that non-hybrids (LL and RR) arise from hybrid  hybrid matings, but die off during larval stages (Christiansen et al, 2005;Arioli, 2007, Chapter 3). The inviability of RR offspring from hybrid  hybrid matings in the L-E system arises from the diploid hybrids' clonal mode of reproduction (Vorburger, 2001a), but this explanation cannot hold for all-hybrid populations where recombination between the two Ls occurs in LLR frogs and between the two Rs in LRR frogs (Christiansen and Reyer, 2009). An alternative hypothesis is that genetic diversity in the L and R genomes within all-hybrid populations is so low that, despite regular recombination within them, LL and RR offspring nevertheless become homozygous for a sufficient number of recessive deleterious mutations to kill them.…”