The unexpected mating system of the androdioecious barnacle Chelonibia testudinaria (Linnaeus 1758)

Androdioecy was first described by Darwin in his seminal work on barnacle diversity; he identified males and hermaphrodites in the same reproductive population. Today, we realize that many androdioecious plants and animals share astonishing similarities, particularly with regard to their evolutionary history and mating system. Notably, these species were ancestrally dioecious, and their mating system has the following characteristics: hermaphrodites self‐fertilize frequently, males are more successful in large mating groups, and males have a mating advantage. A male mating advantage makes androdioecy more likely to persist over evolutionary times. Androdioecious barnacles, however, appear to persist as an outlier with a different evolutionary trajectory: they originate from hermaphroditic species. Although sexual systems of androdioecious barnacles are known, no information on the mating system of androdioecious barnacles is available. This study assessed the mating system of the androdioecious barnacle Chelonibia testudinaria. In contrast to other androdioecious species, C. testudinaria does not self‐fertilize, males do not have a mating advantage over hermaphrodites, and the average mating group is quite small, averaging only three individuals. Mating success is increased by proximity to the mate and penis length. Taken together, the mating system of C. testudinaria is unusual in comparison with other androdioecious plants and animals, and the lack of a male mating advantage suggests that the mating system alone does not provide an explanation for the maintenance of androdioecy in this species. Instead, we propose that sex‐specific life history equalizes male and hermaphroditic overall fitness.     

Effect of recurrent selfing on inbreeding depression and mating system evolution in an autopolyploid plant

Genome duplication resulting in polyploidy can have significant consequences for the evolution of mating systems. Most theory predicts that self‐fertilization will be selectively favored in polyploids; however, many autopolyploids are outcrossing or mixed‐mating. Here, we examine the hypothesis that the evolution of selfing is restricted in autopolyploids because the genetic cost of selfing (i.e., inbreeding depression) increases monotonically with successive generations of inbreeding. Using the herbaceous, autotetraploid plant Chamerion angustifolium, we generated populations with different inbreeding coefficients (F= 0, 0.17 and 0.36) through three consecutive generations of selfing and compared their magnitudes of inbreeding depression in a common environment. Mating system estimates for four natural populations confirmed that tetraploid selfing rates (s_m= 0.25, SE = 0.02) are similar to those of diploids (s_m= 0.12, SE = 0.12; F_1,2= 1.34, P= 0.37) indicating that both cytotypes are predominantly outcrossing. Compared to an outbred control line, mean inbreeding depression for seed production, survival, and height (vegetative and total) in the inbred line differed among generations (inbreeding coefficients). Across all stages, inbreeding depression (relative to control) was positively related to generation (inbreeding coefficient). Although the initial costs of inbreeding in extant and newly synthesized polyploids may be low compared to diploids, the monotonic increase in inbreeding depression with repeated inbreeding may limit the extent to which selfing variants are favored.     

Inbreeding depression and heterosis in populations of Schiedea viscosa, a highly selfing species

Progeny from self-pollinations and intrapopulation crosses were examined in Schiedea viscosa to determine the extent of inbreeding depression in this highly selfing species. Progeny of interpopulation crosses were also investigated to determine whether deleterious alleles have been fixed in populations of S. viscosa. There was no inbreeding depression at early life history stages, including seeds per capsule, seed mass, or germination. Inbreeding depression was detected for the later life history stage of fruit biomass, although not for survival or life span. Heterosis for vegetative biomass and fruit biomass was detected in progeny from crosses between populations. Levels of inbreeding depression in S. viscosa are low relative to out-crossing species of Schiedea, especially when early life history stages are compared.     

A field test of a model for the stability of androdioecy in the freshwater shrimp,Eulimnadia texana

The evolution of hermaphroditism from dioecy is a poorly studied transition. Androdioecy (the coexistence of males and hermaphrodites) has been suggested as an intermediate step in this evolutionary transition or could be a stable reproductive mode. Freshwater crustaceans in the genus Eulimnadia have reproduced via androdioecy for 24+ million years and thus are excellent organisms to test models of the stability of androdioecy. Two related models that allow for the stable maintenance of males and hermaphrodites rely on the counterbalancing of three life history parameters. We tested these models in the field over three field seasons and compared the results to previous laboratory estimates of these three parameters. Male and hermaphroditic ratios within years were not well predicted using either the simpler original model or a version of this model updated to account for differences between hermaphroditic types (‘monogenic’ and ‘amphigenic’ hermaphrodites). Using parameter estimates of the previous year to predict the next year's sex ratios revealed a much better fit to the original relative to the updated version of the model. Therefore, counter to expectations, accounting for differences between the two hermaphroditic types did not improve the fit of these models. At the moment, we lack strong evidence that the long‐term maintenance of androdioecy in these crustaceans is the result of a balancing of life history parameters; other factors, such as metapopulation dynamics or evolutionary constraints, may better explain the 24+ million year maintenance of androdioecy in clam shrimp.     

Evolutionary dynamics of mating system shifts in Arabidopsis lyrata

Outcrossing is the prevalent mode of reproduction in plants and animals despite its substantial costs, while selfing and mixed mating occur at much lower frequency. Comparative research on plants has demonstrated the lability of self‐incompatibility, but there is little information about the transition on a within‐species level from self‐incompatibility to predominant selfing. We studied variation in mating system among 18 populations of Arabidopsis lyrata within a phylogenetic context to shed light on the evolution of selfing. Realized and potential mating systems were assessed by genetic analysis with microsatellite markers and hand‐self‐pollinations on 30 plants from each population. The fraction of self‐incompatible plants in a population was highly correlated with the outcrossing rate, showing that the spread of self‐compatibility is accompanied by or soon followed by an increase in the rate of selfing. The four predominantly selfing populations (outcrossing rates < 0.25) fell into more than one phylogenetic cluster, suggesting that the transition to selfing occurred more than once independently. Hence, A. lyrata offers an opportunity for the comparative analysis of outcrossing as a predominant mode of reproduction in plants and of the causes of the shift to selfing.     

Family level inbreeding depression and the evolution of plant mating systems

Variation in the magnitude of inbreeding depression (ID) among families may have important consequences for mating system evolution. Experimental studies have shown that such variation is a common feature of natural plant populations. Unfortunately, the genetic and evolutionary significance of family level estimates remains obscure. Almost any kind of genetic variation will generate differences in ID among families, and as a consequence, a non-zero variance in family level ID is not sufficient to distinguish genetic architectures with wholly different implications for mating system evolution. Quantitative genetic methods provide a means to extract more information from ID experiments. Estimates of quantitative genetic variance components directly inform questions about the genetic basis of ID and should ultimately allow tests of alternative theories of mating system evolution.     

Inbreeding under a cyclical mating system

Summary General recursion formulae for the coefficient of inbreeding under a cyclical mating system were derived in which one male and one female are selected from each of the n families per generation (population size N = 2 n). Each male is given the family number of his sire in each generation, while his mate comes from another family, varying systematically in different generations. Males of the r-th family in generations 1, 2, 3,..., t = n–1 within each cycle mate with females from families r+1, r+2, r+3,..., r+t to produce generations 2, 3, 4,..., t+1=1, respectively. The change in heterozygosity shows a cyclical pattern of rises and falls, repeating in cycles of n–1 generations. The rate of inbreeding oscillates between <-3% to >6% in different generations within each cycle, irrespective of the population size. The average rate of inbreeding per generation is approximately 1/[4 N-(Log₂N+1)], which is the rate for the maximum avoidance of inbreeding. The average inbreeding effective population size is approximately 2 N–2.     

Plant mating systems affect adaptive plasticity in response to herbivory

The fitness consequences of mating system variation (e.g. inbreeding) have been studied for at least 200 years, yet the ecological consequences of this variation remain poorly understood. Most plants are capable of inbreeding, and also exhibit a remarkable suite of adaptive phenotypic responses to ecological stresses such as herbivory. We tested the consequences of experimental inbreeding on phenotypic plasticity in resistance and growth (tolerance) traits in Solanum carolinense (Solanaceae). Inbreeding reduced the ability of plants to up‐regulate resistance traits following damage. Moreover, inbreeding disrupted growth trait responses to damage, indicating the presence of deleterious mutations at loci regulating growth under stress. Production of the phytohormones abscisic and indole acetic acid, and wounding‐induced up‐regulation of the defence signalling phytohormone jasmonic acid were all significantly reduced under inbreeding, indicating a phytohormonal basis for inbreeding effects on growth and defence trait regulation. We conclude that the plasticity of induced responses is negatively affected by inbreeding, with implications for fragmented populations facing mate limitation and stress as a consequence of environmental change.     

Predominance of outcrossing in Lymnaea stagnalis despite low apparent fitness costs of self-fertilization

We have quantified the natural mating system in eight populations of the simultaneously hermaphroditic aquatic snail Lymnaea stagnalis, and studied the ecological and genetic forces that may be directing mating system evolution in this species. We investigated whether the natural mating system can be explained by the availability of mates, by the differential survival of self- and cross-fertilized snails in nature, and by the effects of mating system on parental fecundity and early survival. The natural mating system of L. stagnalis was found to be predominantly cross-fertilizing. Density of snails in the populations had no relationship with the mating system, suggesting that outcrossing rates are not limited by mate availability at the population densities observed. Contrary to expectations for outcrossing species, we detected no evidence for inbreeding depression in survival in nature with inferential population genetic methods. Further, experimental manipulations of mating system in the laboratory revealed that self-fertilization had no effect on parental fecundity, and only minor effects on offspring survival. Predominance of cross-fertilization despite low apparent fitness costs of self-fertilization is at odds with the paradigm that high self-fertilization depression is necessary for maintenance of cross-fertilization in self-compatible hermaphrodites.     

Male mating strategies and the mating system of great-tailed grackles

Great-tailed grackles (Quiscalus mexicanus) are sexually dimorphic,dichromatic, colonially nesting blackbirds. In this study, males pursued three basic types of conditional mating strategies,each of which employed a different set of mating tactics. Territorialmales defended one or more trees in which several females nested.They achieved reproductive success by siring the offspringof their social mates and through extrapair fertilization.Resident males lived in the colony but did not defend territoriesor have social mates. Transient males passed through the colony, staying no more than a few days, and probably visited more thanone colony. Residents appeared to queue for access to territories,but transients did not. Residents and transients gained allpaternity through extrapair fertilizations and provided noparental care. Territorial males sired the majority of offspring,but residents and transients also sired small numbers of nestlings. Territorial males were larger and had longer tails than nonterritorialmales. The number of social mates was related to body size,and males that sired nestlings were heavier and had longertails than males with no genetic reproductive success. Malesthat gained paternity through extrapair fertilization wereheavier and had longer tails than males that did not. The matingsystem of great-tailed grackles can best be categorized as "non-faithful-female frank polygyny."     

Inbreeding depression in two species of Mimulus (Scrophulariaceae) with contrasting mating systems

We examined the effect of self- and cross-pollination on germination success, flowering probability, pollen and ovule production, survivorship, and adult aboveground biomass in two species of Mimulus with contrasting mating systems: the highly seifing M. micranthus and an outcrossing population of M. guttatus. Cross-pollinations were performed both within and between populations in order to examine the scale at which the genetic load is distributed. We found significant inbreeding depression in M. guttatus in four of the six traits, with the highest inbreeding depression observed in biomass (68% and 69% based on within- and between-population crosses, respectively) and lowest in ovule production (21% based on between-population crosses only). M. micranthus displayed significant inbreeding depression in only two of the six traits examined. Again, we observed the highest inbreeding depression in biomass (47–60% based on within- and between-population crosses, respectively), but both traits showing significant differences between self and outcross progeny expressed lower inbreeding depression than in M. guttatus. We detected no significant inbreeding depression for either pollen or ovule production in M. micranthus. An estimate of total inbreeding depression based on the multiplicative effects of all traits was also lower in M. micanthus than∗∗∗ in M. guttatus. Our results are consistent with the expected purging of genetic load in populations with high selfing rates. The absence of inbreeding depression in M. micranthus pollen and ovule production, two traits with strong links to fitness in a selfing annual, further suggests the important role of directional selection in determining the population's genetic load. Comparison of cross-pollinations made within and between populations revealed little evidence of divergence of genetic load among the M. micranthus and M. guttatus populations examined.     

BEST OF BOTH WORLDS? ASSOCIATION BETWEEN OUTCROSSING AND PARASITE LOADS IN A SELFING FISH

Mixed-mating strategies (i.e., intermediate levels of self-fertilization and outcrossing in hermaphrodites) are relatively common in plants and animals, but why self-fertilization (selfing) rates vary so much in nature has proved difficult to explain. We tested the hypothesis that parasites help maintain mixed-mating using a partially selfing fish (Kryptolebias marmoratus) as a model. We show that outcrossed progeny in the wild are genetically more diverse and less susceptible to multiple parasite infections than their selfed counterparts. Given that outcrossing in K. marmoratus can only be attained by male-hermaphrodite matings, our data provide an explanation for the coexistence of males and hermaphrodites in androdioecious species where hermaphrodites are unable to outcross among themselves. Moreover, our study provides evidence that parasites contribute to maintaining mixed-mating in a natural animal population.     

Estimation of mating systems in Short and Tall ecomorphs of the coral Favia fragum

We used 15 microsatellite markers to estimate the selfing rate (s), outcrossing rate (t_O) and hybridization between partially sympatric ecomorphs (t_H) of the coral Favia fragum. Genotyping of progeny arrays revealed complete self‐fertilization in the Tall ecomorph and low outcrossing (t_O + t_H < 1%) in the Short ecomorph. Further, all larvae could be assigned with high probability to the same population as their parental dam, indicating no hybridization between ecomorphs (t_H = 0). Despite low ecological estimates of outcrossing, Q values from highly structured adult populations indicated that 9% of the adult samples were the products of outcrossing, and an additional 11% were hybrids. Reproductive isolation appears to have a strong geographical component, as we did not detect hybrids at a second site where the two ecomorphs were distributed in complete microallopatry. Adult estimates of gene flow within ecomorphs may be positively biased by ecomorph‐specific patterns of inbreeding depression, but cryptic gene flow between ecomorphs is most likely explained by undetected outcrossing and the fact that hybrid lineages persist after repeated generations of self‐fertilization. Our microsatellite data show that phenotypic differences between ecomorphs are maintained in sympatry despite evidence for hybridization.     

Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes

We combined experimental and comparative techniques to study the evolution of mating behaviors within in a clade of 15 water striders (Gerris spp.). Superfluous multiple mating is costly to females in this group, and consequently there is overt conflict between the sexes over mating. Two alternative hypotheses that could generate interspecific variation in mating behaviors are tested: interspecific variation in optimal female mating rate versus sexually antagonistic coevolution of persistence and resistance traits. These potentially coevolving traits include male grasping and female antigrasping structures that further the interests of one sex over the other during premating struggles. Both processes are known to play a role in observed behavioral variation within species. We used two large sets of experiments to quantify behavioral differences among species, as well as their response to an environmentally (sex-ratio) induced change in optimal female mating rate. Our analysis revealed a large degree of continuous interspecific variation in all 20 quantified behavioral variables. Nevertheless, species shared the same set of behaviors, and each responded in a qualitatively similar fashion to sex-ratio alterations. A remarkably large proportion (> 50%) of all interspecific variation in the magnitude of behaviors, including their response to sex ratio, could be captured by a single multivariate axis. These data suggest tight coevolution of behaviors within a shared mating system. The pattern of correlated evolution was best accounted for by antagonistic coevolution in the relative abilities of each sex to control the outcome of premating struggles. In species where males have a relative advantage, mating activity is high, and the opposite is found in species where females have gained a relative advantage. Our analyses also suggested that evolution has been unconstrained by history, with no consistent evolutionary tendency toward or away from male or female relative advantage.     

因子与巢式交配设计群体近交率的比较研究

探讨了因子和巢式交配设计群体近交率的形成机理,结果表明,这两种交配设计群体结构本身并不导致基近交率累积的差异。在育种选择情况下因子交配设计比巢式设计群体的近交率上升慢,而在完全随机留种和限制随机种情形这两种酱地群体近交率的影响没有差异,但在交配设计情况下,限制随机留种比完全随机留有有交地控制群体近交率的提高。这一结果显示,在动物的家畜遗传留种比完全随机留各 效地控制群体近交率的提高。这一结果显示,     

Flexible mating: cross-pollination affects sex-expression in a marine clonal plant

Many functionally hermaphroditic plants have evolved mechanisms to reduce interference between the sex functions and to optimize reproductive output. In addition to physical mechanisms such as the spatial (herkogamy) and temporal (dichogamy) separation of male and female functions, plasticity in sex expression by means of mate-recognition (flexible mating) could be important in plants with variable access to cross-pollen. This applies particularly to clonal plants because of their modular growth form. We experimentally tested for the effects of pollen source and vegetative neighbourhood on instantaneous sex ratio and seed production in the self-compatible clonal marine angiosperm Zostera marina L. To this end, we exposed the (monoecious) flowering shoots to self and cross-pollen and to neighbourhoods of their own and a mix of foreign vegetative shoots. Flowering shoots that had been exposed to cross-pollen showed (1) a significantly lower female/male ratio at peak flowering, evidence for mate-recognition, and (2) a significantly higher seed set by the end of the season. Both effects were independent of the genetic composition of their vegetative neighbourhood. The results suggest that Z. marina maintains a cryptic self-incompatibility system not previously described for angiosperms with sub-aqueous pollination. In Z. marina, and possibly other self-compatible clonal plant species, mate-recognition could be a means of increasing the out-crossing probability for flowering shoots with central positions within their clone.     

Genetic diversity,sexual condition,and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat‐mosses

In bryophytes, the possibility of intragametophytic selfing creates complex mating patterns that are not possible in seed plants, although relatively little is known about patterns of inbreeding in natural populations. In the peat‐moss genus Sphagnum, taxa are generally bisexual (gametophytes produce both sperm and egg) or unisexual (gametes produced by separate male and female plants). We sampled populations of 14 species, aiming to assess inbreeding variation and inbreeding depression in sporophytes, and to evaluate correlations between sexual expression, mating systems, and microhabitat preferences. We sampled maternal gametophytes and their attached sporophytes at 12–19 microsatellite loci. Bisexual species exhibited higher levels of inbreeding than unisexual species but did generally engage in some outcrossing. Inbreeding depression did not appear to be common in either unisexual or bisexual species. Genetic diversity was higher in populations of unisexual species compared to populations of bisexual species. We found a significant association between species microhabitat preference and population genetic diversity: species preferring hummocks (high above water table) had populations with lower diversity than species inhabiting hollows (at the water table). We also found a significant interaction between sexual condition, microhabitat preference, and inbreeding coefficients, suggesting a vital role for species ecology in determining mating patterns in Sphagnum populations. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 96–113.     

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

Parasite‐mediated selection is one of the main drivers of genetic variation in natural populations. The persistence of long‐term self‐fertilization, however, challenges the notion that low genetic variation and inbreeding compromise the host's ability to respond to pathogens. DNA methylation represents a potential mechanism for generating additional adaptive variation under low genetic diversity. We compared genetic diversity (microsatellites and AFLPs), variation in DNA methylation (MS‐AFLPs), and parasite loads in three populations of Kryptolebias hermaphroditus, a predomintanly self‐fertilizing fish, to analyze the potential adaptive value of DNA methylation in relation to genetic diversity and parasite loads. We found strong genetic population structuring, as well as differences in parasite loads and methylation levels among sampling sites and selfing lineages. Globally, the interaction between parasites and inbreeding with selfing lineages influenced DNA methylation, but parasites seemed more important in determining methylation levels at the local scale.     

An analysis of mating biases in trees

Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.