Self-fertilization In Hermaphrodites Research Articles

The evolutionary ecology of inbreeding depression in wild plant populations and its impact on plant mating systems.

Inbreeding depression, the reduced fitness of inbred relative to outbred individuals was described more than two centuries ago, long before the development of population genetics. Its impact is central to evolutionary ecology and the evolution of mating systems, in particular self-fertilization in hermaphrodites. In the first half of the 20th century, population genetics revealed a mechanism for inbreeding depression through homozygosity. Numerous theoretical studies have modeled inbreeding depression as a function of genetic architecture and analyzed how it varies with population selfing rates. A major concept in these models is purging, i.e., the purging of recessive deleterious mutations through inbreeding. Consequently, inbreeding depression is expected to decrease with increasing population selfing rates. Along with these theoretical studies, many experimental studies, particularly on plants, have measured inbreeding depression using experimental crosses or directly in the field. The results of these studies have revealed that the evolutionary ecology of inbreeding depression is difficult to capture and that empirical data do not exactly match model predictions, specifically purging efficacy. In addition, the lability of inbreeding depression in natural populations can qualitatively affect the selective role of inbreeding depression in the evolution of mating systems. Recently, several studies have demonstrated the role of epigenetics in shedding new light on the dynamics of inbreeding depression in natural populations. This review provides a general overview of the studies on inbreeding depression and how various angles can help capture its selective role in natural populations.

Sexual selection and inbreeding: Two efficient ways to limit the accumulation of deleterious mutations.

Theory and empirical data showed that two processes can boost selection against deleterious mutations, thus facilitating the purging of the mutation load: inbreeding, by exposing recessive deleterious alleles to selection in homozygous form, and sexual selection, by enhancing the relative reproductive success of males with small mutation loads. These processes tend to be mutually exclusive because sexual selection is reduced under mating systems that promote inbreeding, such as self‐fertilization in hermaphrodites. We estimated the relative efficiency of inbreeding and sexual selection at purging the genetic load, using 50 generations of experimental evolution, in a hermaphroditic snail (Physa acuta). To this end, we generated lines that were exposed to various intensities of inbreeding, sexual selection (on the male function), and nonsexual selection (on the female function). We measured how these regimes affected the mutation load, quantified through the survival of outcrossed and selfed juveniles. We found that juvenile survival strongly decreased in outbred lines with reduced male selection, but not when female selection was relaxed, showing that male‐specific sexual selection does purge deleterious mutations. However, in lines exposed to inbreeding, where sexual selection was also relaxed, survival did not decrease, and even increased for self‐fertilized juveniles, showing that purging through inbreeding can compensate for the absence of sexual selection. Our results point to the further question of whether a mixed strategy combining the advantages of both mechanisms of genetic purging could be evolutionary stable.

Gynodioecy in Lobelia Siphilitica and L. Spicata (Lobeliaceae) from Western Massachusetts1

Abstract Gynodioecy is a dimorphic breeding system in which male-sterile individuals (i.e., females) coexist with hermaphroditic individuals in populations. Previous studies of two species of Lobelia in North America have documented gynodioecy in parts of their ranges and here, we document gynodioecy for a single population of L. siphilitica and in two populations of L. spicata from western Massachusetts. Our objectives were to (1) determine sex ratios in natural populations of these species, (2) use controlled pollinations to investigate the capacity and extent of self fertilization in hermaphrodites and (3) compare the relative fertility and magnitude of sexual dimorphism in floral morphology between females and hermaphrodites. The frequency of females was only 3% in L. siphilitica, whereas both populations of L. spicata contained 12% females. Hermaphrodites in both species were self-compatible and estimates of mating system parameters confirmed mixed mating in L. spicata. Females of L. spicata had high...

INBREEDING AND OUTBREEDING DEPRESSION IN CAENORHABDITIS NEMATODES

The nematode Caenorhabditis elegans reproduces primarily by self-fertilization of hermaphrodites, yet males are present at low frequencies in natural populations (androdioecy). The ancestral state of C. elegans was probably gonochorism (separate males and females), as in its relative C. remanei. Males may be maintained in C. elegans because outcrossed individuals escape inbreeding depression. The level of inbreeding depression is, however, expected to be low in such a highly selfing species, compared with an outcrosser like C. remanei. To investigate these issues, we measured life-history traits in the progeny of inbred versus outcrossed C. elegans and C. remanei individuals derived from recently isolated natural populations. In addition, we maintained inbred lines of C. remanei through 13 generations of full-sibling mating. Highly inbred C. remanei showed dramatic reductions in brood size and relative fitness compared to outcrossed individuals, with evidence of both direct genetic and maternal-effect inbreeding depression. This decline in fitness accumulated over time, causing extinction of nearly 90% of inbred lines, with no evidence of purging of deleterious mutations from the remaining lines. In contrast, pure strains of C. elegans performed better than crosses between strains, indicating outbreeding depression. The results are discussed in relation to the evolution of androdioecy and the effect of mating system on the level of inbreeding depression.

Sampling from Natural Populations with RNAi Reveals High Outcrossing and Population Structure in Caenorhabditis elegans

Despite a nearly worldwide distribution in nature, Caenorhabditis elegans exhibits low levels of genetic polymorphism, possibly as an indirect consequence of low levels of outcrossing. In the laboratory, Caenorhabditis elegans males are produced at low rates and are steadily eliminated from cultures, so that reproduction happens largely through self-fertilization in hermaphrodites. C. elegans is increasingly the focus of evolutionary research; however, natural outcrossing rates are difficult to measure because mating tests with laboratory strains are usually required to identify C. elegans. We sampled natural populations of C. elegans with an RNA interference (RNAi) assay. Heterozygosities and polymorphism patterns revealed surprisingly high levels of population structure and outcrossing (approximately 22% of individuals are estimated to be the result of outcrossing and not self-fertilization). The finding of strong local population structure, together with low levels of diversity on local and global scales, suggests a metapopulation model of frequent extinction and recolonization of local populations. The occurrence of substantial outcrossing suggests that the extinction of local populations is probably not driven by the accumulation of harmful mutations.

Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances.

Self-incompatibility systems in plants are genetic systems that prevent self-fertilization in hermaphrodites through recognition and rejection of pollen expressing the same allelic specificity as that expressed in the pistils. The evolutionary properties of these self-recognition systems have been revealed through a fascinating interplay between empirical advances and theoretical developments. In 1939, Wright suggested that the main evolutionary force driving the genetic and molecular properties of these systems was strong negative frequency-dependent selection acting on pollination success. The empirical observation of high allelic diversity at the self-incompatibility locus in several species, followed by the discovery of very high molecular divergence among alleles in all plant families where the locus has been identified, supported Wright's initial theoretical predictions as well as many of its later developments. In the last decade, however, advances in the molecular characterization of the incompatibility reaction and in the analysis of allelic frequencies and allelic divergence from natural populations have stimulated new theoretical investigations that challenged some important assumptions of Wright's model of gametophytic self-incompatibility. We here review some of these recent empirical and theoretical advances that investigated: (i) the hypothesis that S-alleles are selectively equivalent, and the evolutionary consequences of genetic interactions between alleles; (ii) the occurrence of frequency-dependent selection in female fertility; (iii) the evolutionary genetics of self-incompatibility systems in subdivided populations; (iv) the evolutionary implications of the self-incompatibility locus's genetic architecture; and (v) of its interactions with the genomic environment.

Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating.

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny. However, self-fertilization is common in plants; 20% are highly selfing and 33% are intermediate between selfing and outcrossing. Darwin proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.

The Evolution and Maintenance of Androdioecy

▪ Abstract Examples of androdioecy, the coexistence of males and hermaphrodites, was unknown when the subject was last reviewed about two decades ago. Since then, several examples have been discovered in both plants and animals, and we are now in a position to reappraise theoretical work on the subject. Whereas early ideas were framed largely in terms of the invasion of males into hermaphroditic populations, all of the clearest examples of androdioecy now known appear to have evolved from dioecy. There are strong indications that this has occurred repeatedly as a result of the selection of self-fertile hermaphroditism for reproductive assurance during colonization. Male frequencies in these species are highly variable, self-fertilization in hermaphrodites is delayed, and mating opportunities appear to depend strongly on population density. Results from theoretical work on the evolution and maintenance of androdioecy in single populations and in metapopulations are summarized, and several case studies of androdioecious plants and animals are reviewed.

Gynodioecy in Silene vulgaris (Caryophyllaceae): Progeny Success, Experimental Design, and Maternal Effects

This study documents the comparative success of seeds and seedlings of the perennial gynodioecious-gynomonoecious weed, Silene vulgaris, in the greenhouse. The importance of experimental design is stressed by comparing two different statistical analyses of the data. Seeds were obtained from artificial pollinations in the field: self-fertilization of hermaphrodites, and cross-fertilizations of both hermaphrodites and females. One-way analysis of variance using progeny type (selfed hermaphrodites, outcrossed hermaphrodites, and outcrossed females) as the treatment effect for each seed and seedling variable showed statistically discernable differences among progeny from different cross types. The significance of this type of ANOVA resulted from a reduced error term and positively-biased F ratios. A factorial design showed no significant differences due to type of progeny in seed mass, days to germination, leaf number, area, or biomass at six weeks of age. There were, however, significant differences among seeds attributable to maternal parent for all seed and seedling variables. A higher proportion of seeds from outcrossed individuals germinated compared to that from self-fertilization. When the data were analyzed to include and partition all sources of variation, differences among offspring appeared during germination, rather than during later development. Seed mass, cross type, and sex of maternal parent all significantly affected the likelihood of germination; however, they had decreasing predictive power, respectively. Inbreeding depression in Silene vulgaris may help maintain gynodioecy; however, the pleiotropic effects of both nuclear and cytoplasmic genes for sex expression also may affect fitness and the maintenance of females.

Variability in humoral responses to DNP-KLH of rainbow trout ( [formula omitted]). Comparison of antibody kinetics and immunoglobulins spectrotypes between normal trouts and trouts obtained by gynogenesis or self-fertilization

The anti-DNP antibody responses were compared between conventional trouts produced in fishfarm and trouts experimentally obtained by self-fertilization of hermaphrodites or by gynogenesis. The variability of anti-DNP antibody titres was equivalent between normal and gynogenetic fish, but significantly reduced for fish obtained by self-fertilization. Isoelectrofocusing analysis of individually-isolated anti-DNP antibodies indicate low molecular heterogeneity but large variability between conventional trouts. Almost complete sharing of individual spectrotypes was observed between self-fertilized fish and large similarities between gynogenetics animals. These results suggest that the intensity of antibody synthesis in trout is under a complex genetic control, even in inbred animals expressing large similarities in their antibody repertoires.

The genetics and evolution of gynodioecy in Nemophila menziesii (Hydrophyllaceae)

Nemophila menziesii typically bears perfect, protandrous. self-compatible but predominantly outcrossed flowers. In one population of Nemophila menziesii var. intermedia at Point Reyes, California, approximately 25% of the plants are completely male sterile. The flowers of these pistillate plants possess only small rudiments of stamens and lack anthers entirely. This phenotype is constant in nature as well as under cultivation. Male sterility appears to be inherited cytoplasmically, but there is at least one nuclear fertility-restoring allele in the population. The fertility-restoring allele may be at a single multiallelic locus, recessive to one nonfertility-restoring allele and dominant to another nonfertility-restoring allele, or there may be fertility-restoring alleles present at two or more loci. The population carries a significant load of deleterious recessive alleles at other loci, as evidenced by floral abnormalities and partial pollen abortion in some of the progeny from selfed hermaphrodites. Male sterility appears to be maintained in this population because the obligately outcrossed male steriles produce progeny which are more fit than the progeny produced from selfed hermaphrodites. Self-fertilization of hermaphrodites is probably higher in this population than in most populations of the species because the oligolectic-pollen-collecting bees, which are the normal pollinators of N. menziesii, are not present at this locality. Gynodioecy probably became selectively advantageous when the outcrossing ancestors of this population were subjected to drastic increases in the rate of self-fertilization owing to changes in pollinator fauna.