Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why

Jarne, Philippe; Vianey‐Liaud, Monique; Delay, Bernard

doi:10.1111/j.1095-8312.1993.tb00893.x

Cited by 117 publications

(35 citation statements)

References 112 publications

(76 reference statements)

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“…Indeed, using a more robust method to estimate selfing rates based on microsatellites, David et al (2007) showed that hermaphroditic basommatophoran snails lack individuals that have a mixed breeding system (Escobar et al 2011). This is in line with behavioural studies showing that, although many outcrossing hermaphroditic gastropods may be able to self (Jarne and Delay 1991; Jarne et al 1993), 1) natural populations appear primarily or entirely outcrossing (Jarne and Städler 1995), 2) offspring produced by isolated individuals suffer from strong inbreeding depression (Escobar et al 2011), and 3) individuals immediately switch from self‐fertilization to outcrossing when provided with a partner (reviewed by Jordaens et al 2007). Other species appear to be strictly self‐fertilizing and suffer from strong outbreeding depression (Escobar et al 2011).…”

supporting

confidence: 63%

Mixed breeding system in the hermaphroditic land slugArion intermedius(Stylommatophora, Arionidae)

et al. 2013

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Theory suggests that hermaphroditic plants and animals should be either entirely outcrossing or entirely selfing. As such, very few hermaphroditic plants and basommatophoran snails have a mixed breeding system. However, reliable estimates of selfing rates are lacking for most hermaphroditic animals. This partly prevents to delineate the relative contributions of the selective factors that determine selfing and outcrossing rates in hermaphroditic animal taxa. Here, we studied the population genetic structure of, and breeding system in, 11 populations of the hermaphroditic land slug Arion intermedius using five polymorphic microsatellite loci. Moreover, genotype frequencies deviated significantly from Hardy-Weinberg equilibrium expectations for most of the loci in all populations suggesting some level of selfing. Estimates of the selfing level s, suggest moderate levels of outcrossing (mean s based on FIS = 0.84; mean s based on the two-locus heterozygosity disequilibrium = 0.20, or with a ML approach = 0.22). Our study therefore suggests that A. intermedius has a mixed breeding system. A re-analysis of allozyme data from another arionid slug ( subgenus Carinarion) indicates that mixed breeding may be more common in arionid slugs than hitherto was assumed. These results seem therefore at variance with current theoretical and empirical predictions and opens perspectives for the study on the evolutionary factors driving mixed breeding systems in animals.

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supporting

confidence: 63%

Mixed breeding system in the hermaphroditic land slugArion intermedius(Stylommatophora, Arionidae)

et al. 2013

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“…Hermaphroditism and self-fertilization are common among the vascular plants (50) but proportionally rarer among animal species. Nevertheless, several animal phyla, such as mollusks, include both dioecious and hermaphroditic groups (51,52) in which it should prove profitable to investigate the evolutionary forces acting on rate of self-fertilization. Testing sex-allocation theory in plants often involves measuring investment in attractive structures and then either assigning a fraction of the investment to male and female function (53) or determining the effects of attraction on success through male function, female function, and self-fertilization (15).…”

Section: Discussionmentioning

confidence: 99%

Negative correlation between male allocation and rate of self-fertilization in a hermaphroditic animal

Johnston

Das

Hoeh

1998

Proc. Natl. Acad. Sci. U.S.A.

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Sex-allocation theory predicts that the evolution of increased rates of self-fertilization should be accompanied by decreased allocation to male reproduction (sperm production and broadcast). This prediction has found support in plants but has not previously been tested in animals, which, in contrast to biotically pollinated plants, are free of complications associated with incorporating the costs of attractive structures such as petals. Here we report rates of selffertilization as well as proportional allocation to male reproductive tissues within populations of the simultaneous hermaphrodite Utterbackia imbecillis, a freshwater mussel. Individuals from populations with higher selfing rates devoted a lower proportion of reproductive tissue to sperm production (correlation ‫؍‬ ؊0.99), in support of theory.The evolutionary theory of sex allocation is particularly amenable to experimental analysis because its predictions are framed in terms of offspring numbers or energy devoted to male and female reproductive processes (1). Much of the theory is directed at understanding sex-allocation patterns within and among taxa based on the principle of optimization by natural selection (2-8). The theory applies both to sex ratios of offspring in dioecious organisms as well as to the proportion of reproductive energy devoted to each sexual function in hermaphrodites. For hermaphrodites practicing some selffertilization, theory predicts that higher population-level selfing rates should select for lower proportional investment in male function (sperm production) (3, 5, 9-11). This prediction has not previously been tested in animals. Theoretical predictions as well as experimental tests of sex allocation should be more straightforward in animals than in biotically pollinated plants, where the costs and benefits of pollinator attraction must be quantified. Among animals, experimental tests should be most straightforward in groups that do not engage in behaviors, such as egg trading (12, 13), that might be open to cheating. Here we report rates of self-fertilization as well as proportional allocation to male reproductive tissues within populations of the simultaneous hermaphrodite Utterbackia imbecillis, a freshwater mussel.The proportion of reproductive energy optimally devoted to male versus female function in a hermaphrodite should depend on several factors, including the population selfing rate and the shapes of curves relating allocation to sex-specific fertility. When there is no self-fertilization, hermaphrodites are expected to devote equal resources to each function whenever the two fitness-gain curves have the same shape; otherwise, optimal allocation is greater in the sex function for which success increases more rapidly with investment (14). As the mean selfing rate of a population increases, however, an individual's opportunity for fitness gain through sperm broadcast is reduced. The energy spent on sperm broadcast would be better spent on female processes, such as production of eggs and maturation of young....

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“…Population data suggest much higher selfing rates in two populations of P. acuta from Lake Geneva ( Monsutti & Perrin, 1999). The sperm transferred during copulation can be stored and used for many weeks (see Jarne et al ., 1993 ; Vianey‐Liaud, 1997). Eggs are laid within a capsule upon available supports (e.g.…”

Section: Methodsmentioning

confidence: 99%

The influence of self-fertilization and grouping on fitness attributes in the freshwater snail Physa acuta: population and individual inbreeding depression

Jarne

Perdieu²,

Pernot

et al. 2000

Journal of Evolutionary Biology

112

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The genetic structure, selfing rate and inbreeding depression of the hermaphroditic freshwater snail Physa acuta were jointly analysed in a population near Montpellier, France. Allozymic markers revealed moderate gene diversity (0.138), and no heterozygote deficiency. The mean outcrossing rate, estimated by using progeny arrays, was 0.9, with substantial variation among families. This also suggests that the number of fathers among outcrossed offspring of a given mother is low. Inbreeding depression was estimated over more than one generation using 83 first‐laboratory‐generation (G1) families. The main parameters measured were parental (G1) fecundity, offspring (G2) survival and fecundity. Size and growth were also monitored. Parental fecundity was analysed under several conditions (isolation, pair and quadruplet outcrossing). The self‐fertilization depression, including parental fecundity, offspring survival and fecundity, was about 0.9 at the population level. The genetic data obtained in the same population indicate a value of about 0.3 using Ritland’s (1990) technique, suggesting that the depression over the whole life‐cyle might be even higher than 0.9. Grouping affected neither fecundity nor self‐fertilization depression. Substantial variation in depression for survival was detected among individuals, from no survival in some selfed families to better survival than that of outbred families in others. The overall result (outbred population structure, high outcrossing rate and high self‐fertilization depression) is consistent with what is expected in large outcrossing populations in which inbreeding depression is maintained by mutation‐selection balance.

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Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why

Cited by 117 publications

References 112 publications

Mixed breeding system in the hermaphroditic land slugArion intermedius(Stylommatophora, Arionidae)

Mixed breeding system in the hermaphroditic land slugArion intermedius(Stylommatophora, Arionidae)

Negative correlation between male allocation and rate of self-fertilization in a hermaphroditic animal

The influence of self-fertilization and grouping on fitness attributes in the freshwater snail Physa acuta: population and individual inbreeding depression

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