Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs ( Rana lessonae , R. esculenta , R. ridibunda )

Reyer, Heinz‐Ulrich; Niederer, Bettina; Hettyey, Attila

doi:10.1007/s00265-003-0635-y

Cited by 24 publications

(19 citation statements)

References 72 publications

(55 reference statements)

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“…A study by Reyer et al (2003) showed no precedence for conspecific sperm over heterospecific sperm when sperm from the two parental species (R. lessonae and R. ridibunda) compete for fertilizations, consistent with the results from this study. However, hybrid R. esculenta males consistently have lower fertilization success in sperm competition trials with the two parental species, but this could not be attributed to the quality of sperm or a taxon-specific eggsperm recognition system (Reyer et al, 2003). Thus, being highly acoustic species, these observations agree with the hypothesis of a perhaps stronger (but unquantified) selection for pre-gametic hybrid avoidance and less opportunity for selection at a gametic compatibility level.…”

Section: Trial Number Proportion Offspring Siredsupporting

confidence: 81%

“…Another wellcharacterized hybrid system is that of the European water frogs, Rana lessonae and R. ridibunda, resulting in the hybrid species R. esculenta (Berger, 1977;Abt and Reyer, 1993;Engeler and Reyer, 2001). A study by Reyer et al (2003) showed no precedence for conspecific sperm over heterospecific sperm when sperm from the two parental species (R. lessonae and R. ridibunda) compete for fertilizations, consistent with the results from this study. However, hybrid R. esculenta males consistently have lower fertilization success in sperm competition trials with the two parental species, but this could not be attributed to the quality of sperm or a taxon-specific eggsperm recognition system (Reyer et al, 2003).…”

Section: Trial Number Proportion Offspring Siredsupporting

confidence: 81%

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Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

2009

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Hybridization between closely related species often leads to reduced viability or fertility of offspring. Complete failure of hybrid offspring (post-zygotic hybrid incompatibilities) may have an important role in maintaining the integrity of reproductive barriers between closely related species. We show elsewhere that in Peron's tree frog, Litoria peronii, males more closely related to a female sire more offspring in sperm competition with a less related rival male. Observations of rare 'phenotypic intermediate' males between L. peronii and the closely related L. tyleri made us suggest that these relatedness effects on siring success may be because of selection arising from risks of costly hybridization between the two species. Here, we test this hypothesis in an extensive sperm competition experiment, which shows that there is no effect of species identity on probability of fertilization in sperm competition trials controlling for sperm concentration and sperm viability. Instead, there was a close agreement between a male's siring success in isolation with a female and his siring success with the same female in competition with a rival male regardless of species identity. Offspring viability and survival, however, were strongly influenced by species identity. Over a 14-day period, hybrid offspring suffered increasing mortality and developed more malformations and an obvious inability to swim and right themselves, leading to compromised probability of survival. Thus, hybridization in these sympatric tree frogs does not compromise fertilization but has a strong impact on offspring viability and opportunity for reinforcement selection on mate choice for conspecific partners.

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Section: Trial Number Proportion Offspring Siredsupporting

confidence: 81%

Section: Trial Number Proportion Offspring Siredsupporting

confidence: 81%

Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

2009

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“…55, instead of the 0.71 reported by Abt (2003), and Bergen et al (1997) found that mating frequencies of E females were directly related to the proportion of L and E males in an experimental population. Moreover, mating frequencies alone may not be a reliable measure of male reproductive success, because E males show varying degrees of reduced fertility, ranging from equal fertilization rates of eggs by E-than by L-sperm to total sterility of E males (Gu¨nther, 1990;Reyer et al, 2003). All these factors will affect a and b and, consequently, the male/female ratio s (see Equation 5 and Fig.…”

Section: Sex Ratiosmentioning

confidence: 96%

“…Empirical studies have shown that the two parameters do, indeed, differ between the sexes. Reproductive success is higher in female than in male R. esculenta due to (a) female avoidance of E males but no male avoidance of E females (Abt andReyer, 1993, Reyer et al, 1999;Roesli and Reyer, 2000;Engeler and Reyer, 2001), (b) higher fecundity of E females mating with L males than of L females mating with E males Reyer et al, 1999), and (c) reduced fertility in hybrid males, ranging from equal fertilization rate of eggs by E-than by L-sperm to total sterility of E males (Gu¨nther, 1990;Reyer et al, 2003). In terms of survival, sex differences in R. esculenta seem to be less pronounced.…”

Section: Introductionmentioning

confidence: 95%

Variation in Sex Ratio and Evolutionary Rate of Hemiclonal Rana esculenta Populations

Som

Reyer

2006

Evol Ecol

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In many plant and animal taxa mutation rates are higher in males than in females. As a result, the evolutionary speed of genes depends on how much time they spend in either sex. Usually, this time differs between genes located on sex chromosomes but not between those on autosomes.Here we present an unusual system with a partially sex-linked inheritance of autosomes: the hemiclonal frog Rana esculenta (E) which is originally a hybrid between the sexual species R. lessonae (L) and R. ridibunda (R). Rana esculenta excludes the L genome prior to meiosis, produces eggs or sperm containing an unrecombined R genome and restores hybridity by mating with R. lessonae ('hybridogenesis'). Matings between L males and E females result in offspring with an even sex ratio, whereas the reverse combination produces only daughters. The extent of the resulting female bias and the proportion that R alleles have spent in either sex depend on the relative survival (b) and the relative reproductive contribution (a) of E males vs. E females. In this paper, we analyze mathematically how different combinations of a and b influence the sex ratio in R. esculenta populations and, combined with the male/female mutation rate ratio (a), the evolutionary rate of the clonally transmitted R genome. We find that this rate is higher than in an asexual population and lower than in a sexual one. Hence, clonal diversity through new mutations is more easily achievable than in purely asexual species. In contrast, the occurrence and accumulation of deleterious mutations is lower than in a comparable sexual species. We conclude that these intermediate mutation rates improve the ecological and evolutionary potential of hemiclonal organisms, and we draw attention to the implications for the use of microsatellites.

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“…Causes of round egg mortality could not be identified, so it is not known to what extend these eggs died for the same reasons as the offspring at later stages, or were unfertilized. However, sperm of R. esculenta have been found less effective in fertilizing eggs than sperm of either parental species (Reyer et al 2003). Even if many of the round eggs were not fertilized, their mortality may therefore also to some extent be ascribed to hybrid load.…”

Section: Hybrid Loadmentioning

confidence: 98%

Reproduction and Hybrid Load in All-Hybrid Populations of Rana Esculenta Water Frogs in Denmark

Christiansen

Fog²,

Pedersen

et al. 2005

Evolution

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All-hybrid populations of the water frog, Rana esculenta, are exceptional in consisting of independently and to some extent sexually reproducing interspecific hybrids. In most of its range R. esculenta reproduces hemiclonally with one of the parental species, R. lessonae or R. ridibunda, but viable populations of diploid and triploid hybrids, in which no individuals of the parental species have been found, exist in the northern part of the range. We test the hypothesis that nonhybrids arise every year in these all-hybrid populations, but die during larval development. Microsatellite markers were used to determine the genotypes of adults and abnormal and healthy offspring in three all-hybrid populations of R. esculenta in Denmark. Of all eggs and larvae, 63% developed abnormally or died, with some being nonhybrid (genomes matching one of the parental species), many being aneuploid (with noninteger chromosome sets), a few being tetraploid, and many eggs possibly being unfertilized. The 37% surviving and apparently healthy froglets were all diploid or triploid hybrids. In all three populations, gametogenesis matched the pattern previously described for all-hybrid R. esculenta populations in which most triploid adults have two R. lessonae genomes. This pattern was surprising for the one population in which triploid adults had two R. ridibunda genomes, because here it leads to a deficiency of gametes with an R. lessonae genome and should compromise the stability of this population. We conclude that faulty gametogenesis and mating between frogs with incompatible gametes induce a significant hybrid load in all-hybrid populations of R. esculenta, and we discuss compensating advantages and potential evolutionary trajectories to reduce this hybrid load.

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Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs ( Rana lessonae , R. esculenta , R. ridibunda )

Cited by 24 publications

References 72 publications

Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

Variation in Sex Ratio and Evolutionary Rate of Hemiclonal Rana esculenta Populations

Reproduction and Hybrid Load in All-Hybrid Populations of Rana Esculenta Water Frogs in Denmark

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