Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids

Hotz, Hansjürg; Semlitsch, Raymond D.; Gutmann, E Va; Guex, Gaston‐Denis; Beerli, Peter

doi:10.1073/pnas.96.5.2171

Cited by 86 publications

(72 citation statements)

References 80 publications

(72 reference statements)

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“…Although the homozygous effects of these mutations are dramatic, their heterozygous effects on fitness appear to be weak. This may in part explain the high ecological success of R. esculenta (Semlitsch 1993), which benefits from heterosis due to its hybrid condition (Hotz et al 1999 …”

Section: Discussionmentioning

confidence: 99%

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

Vorburger

2001

Evolution

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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.

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Section: Discussionmentioning

confidence: 99%

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

Vorburger

2001

Evolution

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“…Heterosis or hybrid vigour is defined as an increased performance of heterozygous offspring relative to its homozygous parents. It is best described and investigated in corn (Comings & MacMurray 2000;Springer & Stupar 2007) but is also documented in the natural populations of other plants (Hansson & Westerberg 2002) and animals (Hotz et al 1999). The molecular basis of heterosis still remains unclear but two main hypotheses have survived the elaborate discussion of the topic (Springer & Stupar 2007).…”

Section: (C) Evolutionary Consequences Of Hybrid Unisexual Reproductionmentioning

confidence: 99%

“…The potential benefit from this 'conserved' heterozygosity may (at least partially) outweigh the disadvantages of clonal reproduction. The advantage of hybrid vigour has been shown in hybridogenetic frogs (Hotz et al 1999) but was so far never considered in studies about the gynogenetic Amazon molly.…”

Section: (C) Evolutionary Consequences Of Hybrid Unisexual Reproductionmentioning

confidence: 99%

The origin and evolution of a unisexual hybrid:Poecilia formosa

Lampert

Schartl

2008

Phil. Trans. R. Soc. B

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Clonal reproduction in vertebrates can always be traced back to hybridization events as all known unisexual vertebrates are hybrids between recognized species or genetically defined races. Interestingly, clonal vertebrates often also rely on interspecific matings for their reproduction because gynogenesis (sperm-dependent parthenogenesis) and hybridogenesis are common modes of propagation. While in most cases these hybridization events leave no hereditary traces in the offspring, occasionally the genome exclusion mechanism fails and either small parts of male genetic material remain inside the oocyte in the form of microchromosomes, or fusion of the sperm nucleus with the oocyte nucleus leads to polyploid individuals. In this review, we highlight the important role of hybridization for the origin and evolution of a unisexual hybrid: the Amazon molly, Poecilia formosa.

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“…The proportion of parental species and hybrids in natural populations depends on the environment. It it hypothesized that this is because hybrids are more tolerant to environmental stress than parental species: E, in contrast to L, appears to produce metamorphs that are better adapted to hypoxic conditions and fungicides ordinarily used in agriculture (Tunner & Nopp 1979, Semlitsch & Reyer 1992, Fioramonti et al 1997, Hotz et al 1999. Because of this apparent dichotomy in susceptibility to environmental variables, the hybridogenetic system may represent an interesting model for examining the ecology of pathogens.…”

Section: Resale or Republication Not Permitted Without Written Consenmentioning

confidence: 99%

Parasitism by Dermocystidium ranae in a population of Rana esculenta complex in Central Italy and description of Amphibiocystidium n. gen.

Pascolini¹,

Daszak²,

Cunningham³

et al. 2003

Dis. Aquat. Org.

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We report the enigmatic parasite Dermocystidium ranae in a green frog population (Solomeo, Umbria, Italy) of the Rana esculenta complex, consisting of the parental species R. lessonae (L) and hybrid form R. esculenta (E). In this population a rapid 50% decline of the parental form L was observed. Large dermal U-shaped cysts of D. ranae were found primarily on the ventral aspect of infected individuals, with a significantly higher incidence of infection in the parental species compared to the clonal hybrid. In each form, however, there was little pathological change associated with infection, and the cause of the recent declines of R. lessonae at this site remains unknown. In this paper we present the first ultrastructural description of an amphibian Dermocystidium sp. and we review the taxonomy of Dermocystidium, Dermosporidium and Dermomycoides spp. from amphibians. We conclude that Dermosporidium multigranulare Bro= & Kulda, 1954 is synonymous with Dermocystidium ranae Guyénot & Naville, 1922 and, due to lack of sufficient differences between genera and significant dissimilarities with fish Dermocystidium spp., the 3 amphibian genera are synonymous. We propose that they should be designated to a new genus, Amphibiocystidium n. gen., and Dermocystidium retained for those species parasitic in fish.KEY WORDS: Amphibian · Rana · Dermocystidium· Amphibiocystidium · Amphibian declines Resale or republication not permitted without written consent of the publisherDis Aquat Org 56: [65][66][67][68][69][70][71][72][73][74] 2003 undergoes a premeiotic or occasionally a prediplotene meiotic endoreduplication (Tunner & Heppich-Tunner 1991) and 2 apparently normal meiotic divisions resulting in functional, genetically identical haploid gametes that contain an unrecombined R genome. Hybridity in these lineages is restored each generation through fertilization of these gametes by gametes from syntopic L. The vast majority of E lineages coexist as sexual parasites with the host species L.The L-E system population is widespread throughout Europe (Uzzell & Berger 1975). The proportion of parental species and hybrids in natural populations depends on the environment. It it hypothesized that this is because hybrids are more tolerant to environmental stress than parental species: E, in contrast to L, appears to produce metamorphs that are better adapted to hypoxic conditions and fungicides ordinarily used in agriculture (Tunner & Nopp 1979, Semlitsch & Reyer 1992, Fioramonti et al. 1997, Hotz et al. 1999. Because of this apparent dichotomy in susceptibility to environmental variables, the hybridogenetic system may represent an interesting model for examining the ecology of pathogens. A hybridogenetic L-E system is present on the Italian peninsula; it is formed by a lessonae-like parental species and its esculenta-like hybrid (Uzzell & Hotz 1979, Uzzell 1983, Günther & Plötner 1994. Previous research on the composition of the hybridogenetic system conducted in the Trasimeno Lake district in Central Italy suggests that t...

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Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids

Cited by 86 publications

References 80 publications

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

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

The origin and evolution of a unisexual hybrid:Poecilia formosa

Parasitism by Dermocystidium ranae in a population of Rana esculenta complex in Central Italy and description of Amphibiocystidium n. gen.

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