Population Rescue through an Increase in the Selfing Rate under Pollen Limitation: Plasticity versus Evolution.

AbstractIncreased rates of self-fertilization offer reproductive assurance when plant populations experience pollen limitation, but self-fertilization may reduce fitness by exposing deleterious mutations. If an environmental change responsible for pollen limitation also induces plastic mating system shifts toward self-pollination, the reproductive assurance benefit and inbreeding depression cost of increased self-fertilization occur immediately, while the benefit and cost happen more gradually when increased self-fertilization occur through evolution. I built eco-evolutionary models to explore the demographic and genetic conditions in which higher self-fertilization by plasticity and/or evolution rescues populations, following deficits due to a sudden onset of pollen limitation. Rescue is most likely under an intermediate level of selfing rate increase, either through plasticity or evolution, and this critical level of selfing rate increase is higher under stronger pollen limitation. Generally, rescue is more likely through plasticity than through evolution. Under weak pollen limitation, rescue by enhanced self-fertilization may mainly occur through purging of deleterious mutations rather than reproductive assurance. The selfing rate increase conferring the highest rescue probability is lower when the initial population size is smaller. This article shows the importance of plasticity during plant population rescue and offers insights for future studies of the evolution of mating system plasticity.

Stigma receptors control intraspecies and interspecies barriers in Brassicaceae.

Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring1. Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen2,3 to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils1,4-6. The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S-locus cysteine-rich protein/S-locus protein 11 (SCR/SP11)2,3 or a signal from UI pollen binds to the SI female determinant S-locus receptor kinase (SRK)2,3, recruits FERONIA (FER)7-9 and activates FER-mediated reactive oxygen species production in SI stigmas10,11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class12-14 from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops.

Genome-wide analysis of the role of DNA methylation in inbreeding depression of reproduction in Langshan chicken.

Inbreeding depression of chicken reproduction is a major concern in the conservation of chicken genetic resources. To investigate the potential DNA methylation sites involved in the inbreeding depression of chicken reproduction, we carried out whole-genome bisulfite sequencing (WGBS) of hypothalamus and ovary tissues from the strongly and weakly inbred Langshan chickens, respectively. 5948 and 4593 differentially methylated regions (DMRs) were identified in the hypothalamus and ovary between the strongly and weakly inbred Langshan chickens, respectively. Large numbers of DMR-related genes (DMGs) were enriched in reproduction-related pathways. By combining the WGBS and transcriptome data, two DMRs in SRD5A1 and CDC27 genes were inferred as the most likely biomarkers of inbreeding depression of reproduction in Langshan chicken. Our study provides the first systematic investigation of the DNA methylation changes in strongly inbred chickens, and extends our understanding of the regulatory mechanisms underlying inbreeding depression in chicken reproduction.

Genetic rescue by distant trees mitigates qualitative pollen limitation imposed by fine-scale spatial genetic structure.

Restricted seed dispersal frequently leads to fine-scale spatial genetic structure (i.e., FSGS) within plant populations. Depending on its spatial extent and the mobility of pollinators, this inflated kinship at the immediate neighbourhood can critically impoverish pollen quality. Despite the common occurrence of positive FSGS within plant populations, our knowledge regarding the role of long-distance pollination preventing reproductive failure is still limited. Using microsatellite markers, we examined the existence of positive FSGS in two low-density populations of the tree Pyrus bourgaeana. We also designed controlled crosses among trees differing in their kinship to investigate the effects of increased local kinship on plant reproduction. We used six pollination treatments and fully monitored fruit production, fruit and seed weight, proportion of mature seeds per fruit, and seed germination. Our results revealed positive FSGS in both study populations and lower fruit initiation in flowers pollinated with pollen from highly-genetically related individuals within the neighbourhood, with this trend intensifying as the fruit development progressed. Besides, open-pollinated flowers exhibited lower performance compared to those pollinated by distant pollen donors, suggesting intense qualitative pollen limitation in natural populations. We found positive fine-scale spatial genetic structure is translated into impoverished pollen quality from nearby pollen donors which negatively impacts the reproductive success of trees in low-density populations. Under this scenario of intrapopulation genetic rescue by distant pollen donors, the relevance of highly-mobile pollinators for connecting spatially and genetically distant patches of trees may be crucial to safeguarding population recruitment.

Standard Deviations: The Biological Bases of Transmission Ratio Distortion.

The rule of Mendelian inheritance is remarkably robust, but deviations from the equal transmission of alternative alleles at a locus [a.k.a. transmission ratio distortion (TRD)] are also commonly observed in genetic mapping populations. Such TRD reveals locus-specific selection acting at some point between the diploid heterozygous parents and progeny genotyping and therefore can provide novel insight into otherwise-hidden genetic and evolutionary processes. Most of the classic selfish genetic elements were discovered through their biasing of transmission, but many unselfish evolutionary and developmental processes can also generate TRD. In this review, we describe methodologies for detecting TRD in mapping populations, detail the arenas and genetic interactions that shape TRD during plant and animal reproduction, and summarize patterns of TRD from across the genetic mapping literature. Finally, we point to new experimental approaches that can accelerate both detection of TRD and characterization of the underlying genetic mechanisms.

The genetic basis of inbreeding depression in potato.

Inbreeding depression confers reduced fitness among the offspring of genetic relatives. As a clonally propagated crop, potato (Solanum tuberosum L.) suffers from severe inbreeding depression; however, the genetic basis of inbreeding depression in potato is largely unknown. To gain insight into inbreeding depression in potato, we evaluated the mutation burden in 151 diploid potatoes and obtained 344,831 predicted deleterious substitutions. The deleterious mutations in potato are enriched in the pericentromeric regions and are line specific. Using three F2 populations, we identified 15 genomic regions with severe segregation distortions due to selection at the gametic and zygotic stages. Most of the deleterious recessive alleles affecting survival and growth vigor were located in regions with high recombination rates. One of these deleterious alleles is derived from a rare mutation that disrupts a gene required for embryo development. This study provides the basis for genome design of potato inbred lines.

Mixed pollen load and late-acting self-incompatibility flexibility in Adenocalymma peregrinum (Miers) L.G. Lohmann (Bignonieae: Bignoniaceae).

Mixed cross and self-pollen load on the stigma (mixed pollination) of species with late-acting self-incompatibility system (LSI) can lead to self-fertilized seed production. This "cryptic self-fertility" may allow selfed seedling development in species otherwise largely self-sterile. Our aims were to check if mixed pollinations would lead to fruit set in LSI Adenocalymma peregrinum, and test for evidence of early-acting inbreeding depression in putative selfed seeds from mixed pollinations. Experimental pollinations were carried out in a natural population. Fruit and seed set from self-, cross and mixed pollinations were analysed. Further germination tests were carried out for the seeds obtained from treatments. Our results confirm self-incompatibility, and fruit set from cross-pollinations was three-fold that from mixed pollinations. This low fruit set in mixed pollinations is most likely due to a greater number of self- than cross-fertilized ovules, which promotes LSI action and pistil abortion. Likewise, higher percentage of empty seeds in surviving fruits from mixed pollinations compared with cross-pollinations is probably due to ovule discounting caused by self-fertilization. Moreover, germinability of seeds with developed embryos was lower in fruits from mixed than from cross-pollinations, and the non-viable seeds from mixed pollinations showed one-third of the mass of those from cross-pollinations. The great number of empty seeds, lower germinability, lower mass of non-viable seeds, and higher variation in seed mass distribution in mixed pollinations, strongly suggests early-acing inbreeding depression in putative selfed seeds. In this sense, LSI and inbreeding depression acting together probably constrain self-fertilized seedling establishment in A. peregrinum.

Evolutionary consequences of ecological factors: pollinator reliability predicts mating-system traits of a perennial plant.

The reproductive-assurance hypothesis predicts that mating-system traits will evolve towards increased autonomous self-pollination in plant populations experiencing unreliable pollinator service. We tested this long-standing hypothesis by assessing geographic covariation among pollinator reliability, outcrossing rates, heterozygosity and relevant floral traits across populations of Dalechampia scandens in Costa Rica. Mean outcrossing rates ranged from 0.16 to 0.49 across four populations, and covaried with the average rates of pollen arrival on stigmas, a measure of pollinator reliability. Across populations, genetically based differences in herkogamy (anther-stigma distance) were associated with variation in stigmatic pollen loads, outcrossing rates and heterozygosity. These observations are consistent with the hypothesis that, when pollinators are unreliable, floral traits promoting autonomous selfing evolve as a mechanism of reproductive assurance. Extensive covariation between floral traits and mating system among closely related populations further suggests that floral traits influencing mating systems track variation in adaptive optima generated by variation in pollinator reliability.

Reproductive success through high pollinator visitation rates despite self incompatibility in an endangered wallflower.

PREMISE OF THE STUDY: Self incompatibility (SI) in rare plants presents a unique challenge-SI protects plants from inbreeding depression, but requires a sufficient number of mates and xenogamous pollination. Does SI persist in an endangered polyploid? Is pollinator visitation sufficient to ensure reproductive success? Is there evidence of inbreeding/outbreeding depression? We characterized the mating system, primary pollinators, pollen limitation, and inbreeding/outbreeding depression in Erysimum teretifolium to guide conservation efforts. METHODS: We compared seed production following self pollination and within- and between-population crosses. Pollen tubes were visualized after self pollinations and between-population pollinations. Pollen limitation was tested in the field. Pollinator observations were quantified using digital video. Inbreeding/outbreeding depression was assessed in progeny from self and outcross pollinations at early and later developmental stages. KEY RESULTS: Self-pollination reduced seed set by 6.5× and quadrupled reproductive failure compared with outcross pollination. Pollen tubes of some self pollinations were arrested at the stigmatic surface. Seed-set data indicated strong SI, and fruit-set data suggested partial SI. Pollinator diversity and visitation rates were high, and there was no evidence of pollen limitation. Inbreeding depression (δ) was weak for early developmental stages and strong for later developmental stages, with no evidence of outbreeding depression. CONCLUSIONS: The rare hexaploid E. teretifolium is largely self incompatible and suffers from late-acting inbreeding depression. Reproductive success in natural populations was accomplished through high pollinator visitation rates consistent with a lack of pollen limitation. Future reproductive health for this species will require large population sizes with sufficient mates and a robust pollinator community.

Reproductive patterns, genetic diversity and inbreeding depression in two closely related Jumellea species with contrasting patterns of commonness and distribution.

BACKGROUNDS AND AIMS: Theory predicts that the long-term persistence of plant populations exposed to size reduction can be threatened by a loss of genetic diversity and increased inbreeding. However, several life-history and ecological traits can influence the response to population size reduction. The reproductive patterns, levels of genetic diversity and magnitude of inbreeding depression of the rare and fragmented Jumellea fragrans and of its widespread congener J. rossii were studied. The aim was to evaluate the effects of over-collection and fragmentation on J. fragrans and to enhance our knowledge of the biology and ecology of the two species, used for their aromatic and medicinal properties on Réunion. METHODS: Hand pollination experiments were conducted to determine the breeding system and to evaluate the potential for inbreeding depression in both species. Nuclear microsatellite markers were used to investigate selfing rates and levels of genetic diversity. KEY RESULTS: Jumellea rossii revealed a mixed-mating system, and inbreeding depression at the germination stage (δ = 0·66). Levels of genetic diversity were relatively high [allelic richness (AR) = 8·575 and expected heterozygosity (He) = 0·673]. In J. fragrans, selfing rates suggest a mainly outcrossing mating system. Genetic diversity was lower than in J. rossii, but not yet critically low (AR = 4·983 and He = 0·492), probably because of the mainly outcrossing mating system and the relatively high density of individuals in the studied population. Jumellea fragrans did not show inbreeding depression, and it is hypothesized that the population had progressively purged its genetic load during successive fragmentation events. CONCLUSIONS: Even if the persistence of the J. fragrans population is not threatened in the short term, its genetic diversity has probably been reduced by fragmentation and over-collection. In situ conservation actions for J. fragrans and ex situ cultivation of both species are recommended in order to meet the demand of local people.