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Excluding insects, hermaphroditism occurs in about one-third of animal species, providing numerous opportunities for the evolution of selfing. Here we provide an overview of reproductive traits in hermaphroditic animal species, review the distribution of selfing rates in animals, and test for ecological correlates of selfing. Our dataset (1342 selfing-rate estimates for 142 species) is 97% based on estimates derived from the analysis of population structure (F(IS)-estimates) using genetic markers. The distribution of selfing is slightly U-shaped and differs significantly from the more strongly U-shaped plant distribution with 47% of animal t-estimates being intermediate (falling between 0.2 and 0.8) compared to 42% for plants. The influence of several factors on the distribution of selfing rates was explored (e.g., number of populations studied per species, habitat, coloniality, sessility, or fertilization type), none of which significantly affect the distribution. Our results suggest that genetic forces might contribute to the evolution of self-fertilization to the same extent in animals and plants, although the high proportion of intermediate outcrossing suggests a significant role of ecological factors (e.g., reproductive assurance) in animals. However, we caution that the distribution of selfing rates in animals is affected by various factors that might bias F(IS)-estimates, including phylogenetic underrepresentation of highly selfing and outcrossing species, various genotyping errors (e.g., null alleles) and inbreeding depression. This highlights the necessity of obtaining better estimates of selfing for hermaphroditic animals, such as genotyping progeny arrays, as in plants.
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PMID:Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. 1708 66

Hermaphroditism allows considerable scope for contributing genes to subsequent generations through various mixtures of selfed and outcrossed offspring. The fitness consequences of different family compositions determine the evolutionarily stable mating strategy and depend on the interplay of genetic features, the nature of mating, and factors that govern offspring development. This theoretical article considers the relative contributions of these influences and their interacting effects on mating-system evolution, given a fixed genetic load within a population. Strong inbreeding depression after offspring gain independence selects for exclusive outcrossing, regardless of the intensity of predispersal inbreeding depression, unless insufficient mating limits offspring production. The extent to which selfing evolves under weak postdispersal inbreeding depression depends on predispersal inbreeding depression and the opportunity for resource limitation of offspring production. Mixed selfing and outcrossing is an evolutionarily stable strategy (ESS) if selfed zygotes survive poorly, but selfed offspring survive well, and maternal individuals produce enough "extra" eggs that deaths of unviable outcrossed embryos do not impact offspring production (reproductive compensation). Mixed mating can also be an ESS, despite weak lifetime inbreeding depression, if self-mating reduces the number of male gametes available for outcrossing (male-gamete discounting). Reproductive compensation and male-gamete discounting act largely independently on mating-system evolution. ESS mating systems always involve either complete fertilization or fertilization of enough eggs to induce resource competition among embryos, so although reproductive assurance is adaptive with insufficient mating, it is never an ESS. Our results illustrate the theoretical importance of different constraints on offspring production (availability of male gametes, egg production, and maternal resources) for both the course and outcome of mating-system evolution, whereas unequal competition between selfed and outcrossed embryos has limited effect. These results also underscore the significance of heterogeneity in the nature and intensity of inbreeding depression during the life cycle for the evolution of hermaphrodite mating systems.
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PMID:Effects of reproductive compensation, gamete discounting and reproductive assurance on mating-system diversity in hermaphrodites. 1806 73

Androdioecy, where males co-occur with hermaphrodites, is a rare sexual system in plants and animals. It has a scattered phylogenetic distribution, but it is common and has persisted for long periods of evolutionary time in branchiopod crustaceans. An earlier model of the maintenance of males with hermaphrodites in this group, by Otto et al. (1993), considered the importance of male-hermaphrodite encounter rates, sperm limitation, male versus hermaphrodite viability and inbreeding depression suffered by selfed progeny. Here I advance this model in two ways: (1) by exploring the conditions that would allow the invasion of hermaphrodites into a dioecious population and that of females into an androdioecious population; and (2) by incorporating a term that accounts for the potential effects of genetic load linked to a dominant hermaphrodite-determining allele in androdioecious populations. The new model makes plausible sense of observations made in populations of the species Eulimnadia texana, one of a number of related species whose common ancestor evolved hermaphroditism (and androdioecy) from dioecy. In particular, it offers an explanation for the long evolutionary persistence of androdioecy in branchiopods and suggests reasons for why dioecy has not re-evolved in the clade. Finally, it provides a rather unusual illustration of the implications of the degeneration of loci linked to a sex-determining locus.
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PMID:Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans. 1828 2

Inbreeding depression is a key factor in the maintenance of separate sexes in plants through selection for the avoidance of self-fertilization. However, very little is known about the levels of inbreeding depression in dioecious species, obviously because it is difficult to self-fertilize males or females. We overcame this problem by clonally propagating males from lineages in a dioecious metapopulation of the European annual plant Mercurialis annua, feminizing some of them and crossing the feminized with the unfeminized clones. Using this method, we compared the fitness of selfed vs outcrossed progeny under field conditions in Spain, where this species grows naturally. Multiplicative inbreeding depression (based on seed germination, early and late survival, seed mass and pollen viability) ranged from -0.69 to 0.82, with a mean close to zero. We consider possible explanations for both the low mean and high variance in inbreeding depression in M. annua, and we discuss the implications of our results for the maintenance of dioecy over hermaphroditism.
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PMID:Inbreeding depression in dioecious populations of the plant Mercurialis annua: comparisons between outcrossed progeny and the progeny of self-fertilized feminized males. 1929 36

Plants exhibit complex mating patterns because of their immobility, hermaphroditism and reliance on vectors for pollen transfer. Research on plant mating attempts to determine who mates with whom in plant populations and how and why mating patterns become evolutionarily modified. Most theoretical models of mating-system evolution have focused on the fitness consequences of selling and outcrossing, stimulating considerable empirical work on the ecology and genetics of inbreeding depression. Less attention has been given to how the mechanics of pollen dispersal influence the transmission of self and outcross gametes. Recent work on the relation between pollen dispersal and mating suggests that many features of floral design traditionally interpreted as anti-selling mechanisms may function to reduce the mating costs associated with large floral displays.
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PMID:Ecology and evolution of plant mating. 2123 65

The influence of outcrossing and pollination biology on the maintenance of hermaphroditism was studied for Schiedea lydgatei (Caryophyllaceae: Alsinoideae), a species endemic to Moloka`i in the Hawaiian Islands. Schiedea lydgatei is the only hermaphroditic species in an otherwise dimorphic clade and hermaphroditism is likely the result of a reversal from a gynodioecious ancestor. Both wind and native moths in the family Pyralidae are responsible for pollination in S. lydgatei. Outcrossing rates were generally high (0.80), especially in years when the greatest number of plants were flowering. The combination of high outcrossing rates and substantial inbreeding depression indicates that at present females would not be favored in the population. Pollination by both wind and insects is consistent with the hypothesis that hermaphroditism is the result of a relatively recent reversal, as the ancestor of S. lydgatei was probably wind pollinated and gynodioecious with few females in the populations. A shift from wind to predominately insect pollination on Moloka`i may have resulted in increased outcrossing rates and prevented the expression of high inbreeding depression among progeny of hermaphrodites, a condition that would select against females and favor a reversal to hermaphroditism. Because few females were likely to have been present in ancestral populations that colonized Moloka`i, founder effect is another potential explanation for loss of females. In either case, current high levels of outcrossing prevent re-establishment of females in populations of S. lydgatei.
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PMID:Pollination biology and outcrossing rates in hermaphroditic Schiedea lydgatei (Caryophyllaceae). 2170 17

Dioecy (gonochorism) is dominant within the Animalia, although a recent review suggests hermaphroditism is also common. Evolutionary transitions from dioecy to hermaphroditism (or vice versa) have occurred frequently in animals, but few studies suggest the advantage of such transitions. In particular, few studies assess how hermaphroditism evolves from dioecy or whether androdioecy or gynodioecy should be an "intermediate" stage, as noted in plants. Herein, these transitions are assessed by documenting the numbers of androdioecious and gynodioecious animals and inferring their ancestral reproductive mode. Both systems are rare, but androdioecy was an order of magnitude more common than gynodioecy. Transitions from dioecious ancestors were commonly to androdioecy rather than gynodioecy. Hermaphrodites evolving from sexually dimorphic dioecious ancestors appear to be constrained to those with female-biased sex allocation; such hermaphrodites replace females to coexist with males. Hermaphrodites evolving from sexually monomorphic dioecious ancestors were not similarly constrained. Species transitioning from hermaphroditic ancestors were more commonly androdioecious than gynodioecious, contrasting with similar transitions in plants. In animals, such transitions were associated with size specialization between the sexes, whereas in plants these transitions were to avoid inbreeding depression. Further research should frame these reproductive transitions in a theoretical context, similar to botanical studies.
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PMID:The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the animalia. 2320 27

Androdioecy (the coexistence of males and hermaphrodites) is considered a transitional state derived from pure hermaphroditism or dioecy, but the processes selecting for this rare breeding system are unclear, particularly in animals. In androdioecious species, the proportion of males in relation to hermaphrodites is usually so reduced that it is not known whether there is scope for mate choice, particularly when simultaneous hermaphrodites can self-fertilize. We investigated the potential role of male mate choice in the persistence of androdioecy in animals using a self-fertilizing androdioecious fish (Kryptolebias marmoratus) as a model. Hermaphrodites preferred to associate with males but showed no preference based on genetic similarity. In contrast, males displayed a strong preference for genetically dissimilar hermaphrodites, based, apparently, on olfactory cues. We suggest that disassortative male mate choice could be a critical factor in stabilizing androdioecy in cases where high selfing rates are associated with inbreeding depression.
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PMID:Choosy males could help explain androdioecy in a selfing fish. 2366 47

The evolutionary transition from hermaphroditism (combined sexes) to dioecy (separate sexes) is associated with whole genome duplication (polyploidy) in several flowering plant genera. Moreover, there is evidence for transitions in the opposite direction, i.e. a loss of dioecy with an increase in ploidy. Here, we review evidence for these associations, synthesize previous ideas on the mechanism underlying the patterns and explore alternative pathways. Specifically, we examine potential ecological and genetic mechanisms, differentiated by whether ploidy or gender (functional sex expression of the plant) changes are the primary cause and whether the effect is direct or indirect. An analysis of 22 genera variable for both ploidy and gender indicates that gender monomorphism (hermaphroditism, monoecy) is more common among diploid than polyploid species, whereas gender dimorphism (dioecy, gynodioecy, subdioecy) is more frequent among polyploid species. The transition from diploid hermaphroditic to polyploid gender-dimorphic taxa may arise directly through changes in gender as a result of genome duplication through genomic rearrangements or homeologous recombination, or changes in gender may result in increased unreduced gamete production leading to polyploid formation. Alternatively, the transition may occur through the indirect effects of genome duplication on mating system and inbreeding depression, which favor selection for unisexuality, or habitat shifts associated with unisexuality may simultaneously cause increased unreduced gamete production. Novel mechanisms for transitions in the opposite direction (from dioecy to hermaphroditism with increase in ploidy) include disruption of genetic sex determination and the benefits of reproductive assurance. We highlight key questions requiring further attention and promising approaches for answering them and better clarifying the genesis of sexual system polyploidy associations. See also the sister article focusing on animals by Wertheim et al. in this themed issue.
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PMID:Revisiting the dioecy-polyploidy association: alternate pathways and research opportunities. 2383 28

Theory and empirical study produce clear links between mating system evolution and inbreeding depression. The connections between mating systems and outbreeding depression, whereby fitness is reduced in crosses of less related individuals, however, are less well defined. Here we investigate inbreeding and outbreeding depression in self-fertile androdioecious nematodes, focusing on Caenorhabditis sp. 11. We quantify nucleotide polymorphism for nine nuclear loci for strains throughout its tropical range, and find some evidence of genetic differentiation despite the lowest sequence diversity observed in this genus. Controlled crosses between strains from geographically separated regions show strong outbreeding depression, with reproductive output of F1s reduced by 36% on average. Outbreeding depression is therefore common in self-fertilizing Caenorhabditis species, each of which evolved androdioecious selfing hermaphroditism independently, but appears strongest in C. sp. 11. Moreover, the poor mating efficiency of androdioecious males extends to C. sp. 11. We propose that self-fertilization is a key driver of outbreeding depression, but that it need not evolve as a direct result of local adaptation per se. Our verbal model of this process highlights the need for formal theory, and C. sp. 11 provides a convenient system for testing the genetic mechanisms that cause outbreeding depression, negative epistasis, and incipient speciation.
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PMID:Outbreeding depression with low genetic variation in selfing Caenorhabditis nematodes. 2415 95


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