Gene transfer by interspecific hybridization in bryophytes

The role of hybridization in evolution has been debated for more than a century regarding bryophytes (mosses, liverworts, and hornworts) as well as most other organisms. Bryophytes have haplodiplontic life cycles with a dominant haploid generation. Hybridization in bryophytes involves fusion of gametes produced by haploid parental gametophytes of different species. The hybrid is thus the short-lived diploid sporophytes, which soon undergoes meiosis prior to forming a large amount of haploid recombinant spores. In this study, two moss species (Homalothecium lutescens and H. sericeum) and three subspecies of liverwort Marchantia polymorpha were investigated for evidence of gene transfer by hybridization.Firstly, we compared the morphology of gametophytes and sporophytes from allopatric and sympatric populations of H. lutescens and H. sericeum. Secondly, we used species-specific SNP markers to estimate the degree of genetic mixing in three generations (i.e., haploid maternal gametophytes, diploid sporophytes, and haploid sporelings) in samples from sympatric populations of H. lutescens and H. sericeum. Thirdly, we assessed fitness traits in relation to the degree of genetic admixture in sporophytes of H. lutescens and H. sericeum, including non-admixed, mildly and strongly admixed genotypes. Finally, we investigated the genome-wide scale phylogenetic relationship between the three subspecies of M. polymorpha to test the hypothesis that subsp. ruderalis has originated as a homoploid hybrid species between subsp. polymorpha and subsp. montivagans. Our study of Homalothecium shows that gametophytes from sympatric populations display intermediate morphology in a number of leaf characters, with the exception for leaf dimensions, which are strikingly smaller than those in allopatric populations. Most sporophytes with intermediate capsule inclination, initially classified as putative hybrids, did not display admixture of SNP markers. Many sporophytes appeared to be secondary hybrids by displaying asymmetrical admixture of SNP markers except five sporophytes, which were found to be primary hybrids. Admixture analyses using SNP markers identified 76 samples (17%) as mildly admixed and 17 samples (3.8%) as strongly admixed. Admixed samples represented all three generations and were found in all sympatric populations. Hybridization and introgression were bidirectional. Admixed sporophytes gave rise to viable recombinant spores and sporelings. Sporophytes with mildly admixed H. lutescens tended to show lower fitness, whereas sporophytes with mildly admixed H. sericeum showed signs of heterosis. Some strongly admixed sporophytes showed high spore counts, intermediate spore diameters and high spore germination rates. Genomic analysis showed three distinct taxa within the M. polymorpha complex, coinciding with the three generally accepted subspecies. All three possible topologies were frequent across the genome but species tree analyses using M. paleacea as outgroup recovered an overall branching order where subsp. montivagans diverged first and subsp. ruderalis and subsp. polymorpha were placed as sister species. The high degree of inconsistent gene trees suggests frequent incomplete lineage sorting (ILS) and/or recent or intermittent introgression. Evidence for recent introgression was found in two samples of M. polymorpha. Remarkably, pseudo-chromosome 2 in subsp. montivagans differed by being more diverged than other parts of the genomes. This could either be explained by specific capture of chromosome 2 from an unknown related species through hybridization or by conservation of chromosome 2 despite intermittent or ongoing introgression affecting more permeable parts of the genomes. A higher degree of chromosomal rearrangement in pseudochromosome 2 of subsp. montivagans provide some evidence for the latter explanation.Our results show that gene transfer between lineages occurs in sympatric populations of both the Marchantia polymorpha complex and among the Homalothecium species. This supports the hypothesis that homoploid hybridization is more widespread among bryophytes than earlier assumed. Moreover, the population-level studies of sympatric populations of H. lutescens and H. sericeum demonstrate that they behave as true hybrid zones, where genetic material is transferred across species boundaries and secondarily backcrossed. Presence of hybrid zones has strong evolutionary implications because genetic material transferred across species boundaries can be directly subject of natural selection in the dominant haploid generation of the bryophyte life cycle, and contribute to local adaptation, survival and speciation

Evidence for interspecific hybridization in bryophytes during pre-molecular and molecular eras

nterspecific hybridization had been long recognized as a widespread evolutionary process in vascular plants. In the present review, we summarize knowledge concerning studies of interspecific hybridization in bryophytes before and after the advent of molecular methods. The available data indicate that hybridization is an important evolutionary phenomenon among bryophytes. evidence for hybridization events before the molecular era is mainly based on studies of intermediacy of parental morphology. The recent molecular marker technology has revolutionized studies of hybridization, generating new insights into the genetic and evolutionary consequences of homoploid and allopolyploid speciation. The current molecular approaches support the prevalence of allopolyploidy in bryophytes. however, we anticipate that homoploid hybridization is under-reported. Finally, we suggest some directions for future studies of hybrid speciation among bryophytes

Life History Traits of the Liverwort Herbivore Scatopsciara cunicularius (Diptera: Sciaridae)

We studied the behavior, life cycle, and reproductive biology of the sciarid fly Scatopsciara cunicularius (Lengersdorf, 1943) under two constant temperatures. The sciarid was reared at 12.3 ± 0.6°C and 22 ± 1.7°C on its host, the liverwort Marchantia polymorpha L. Our results show that the sciarid fly is able to complete its life cycle with liverwort tissue as its only source of food. The egg-laying potential of the insect ranged from 70–174 eggs per female (mean 110 ± 31 eggs). Reproduction was digenic, meaning that one female can produce both male and female progeny. The overall sex ratio did not depart from 1:1, although the progeny sex ratio was highly variable. The developmental period of S. cunicularius was considerably longer in the colder than the warmer temperature. Mean development time of the egg, larva, and pupal stages, and adult longevity in the warm regime was 4, 20, 4, and 5 d, whereas mean development time of each juvenile stage and adult longevity in the cold regime was 13, 95, 11, and 8 d, respectively. The results suggest that the phenology of S. cunicularius is temperature dependent. Scatopsciara cunicularius could constitute a promising agent for biological control of M. polymorpha

The effect of ambient temperature on larvae of Scatopsciara cunicularius (Diptera: Sciaridae) feeding on the thallose liverwort Marchantia polymorpha

Herbivory on liverworts is rarely reported. We studied the effects of feeding by larvae of the sciarid fly Scatopsciara cunicularius on the growth of the thalloid liverwort Marchantia polymorpha at two different constant temperatures, 12°C and 22°C. Larvae reared at the lower temperature fed slower and over a longer period of time, which resulted in more damage and a greater reduction in the growth of the liverwort than that caused by those reared at the higher temperature. The reduction in growth of the liverwort was positively density-dependent in terms of number of larvae at both temperatures. These results indicate that the larvae of S. cunicularius are likely to be an effective means of controlling M. polymorpha, which is a common weed in plant nurseries and greenhouse cultures

Asian openbill stork Anastomus oscitans as a predator of the invasive alien gastropod Pomacea canaliculata in Thailand

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Morphological characters and SNP markers suggest hybridization and introgression in sympatric populations of the pleurocarpous mosses Homalothecium lutescens and H. sericeum

Hybridization in bryophytes involves a fusion of gametes produced by haploid parental gametophytes of different species. The primary hybrid is thus the short-lived diploid sporophyte, which soon undergoes meiosis prior to the formation of large amounts of haploid spores. We compared morphology of gametophytes (branch leaves) and sporophytes (capsule inclination) from sympatric populations and allopatric populations of H. lutescens and H. sericeum. In addition, we used transcriptome data to select 85 nuclear SNP markers that were fixed for alternative alleles in the two species. The SNPs were used to estimate the degree of hybridization in diploid sporophytes. Our study shows that gametophytes from sympatric populations display intermediate morphology in a number of leaf characters, with exception for leaf sizes, which are markedly smaller than those in allopatric populations. None of the 100 sporophytes appeared to be primary hybrids, but 33 displayed admixing—heterozygotic expression of SNP markers or mismatch of occasional markers in homozygous condition—suggesting that extensive introgression takes place in the sympatric populations. Most sporophytes with intermediate capsule inclination, initially classed as putative hybrids, did not display admixture of nuclear SNP markers. Sixty-seven percent of admixed sporophytes have predominantly nuclear SNPs typical for H. lutescens. Our results suggest that interspecific hybridization and bidirectional introgression are relatively common in the studied sympatric populations, giving rise to viable recombinants, but not complete mixing of the parental genomes. Our study is one of the first detailed accounts of hybridization among pleurocarpous mosses, opening for future studies of gene transfer and introgression between bryophyte lineages and its role in local adaptation and long-term evolutionary diversification

Removal of Pb(II) and Cd(II) by Biomass Derived from Broadleaf Cattail and Water Hyacinth

The potential of cattail (Typha latifolia) and water hyacinth (Eichhornia crassipes) biomass to remove Pb and Cd ions from metal solutions was determined. The removal efficiency of Pb and Cd decreased with the increase in the initial concentration of metal aqueous solution but increased with the increased biomass doses. The biosorption was unaffected by the increase in pH from 5.0 to 6.5. Metal removal efficiency increased with increased contact time and then reached equilibrium in about 45 min. Higher qmax (the Langmuir model) and KF (the Freundlich constant) suggest that both cattail and water hyacinth biomass have a greater affinity for Pb(II) than Cd(II). The better fitness of the adsorption kinetics in the pseudo-second-order model than in the pseudo-first-order model indicates that biomass has an inclination toward chemisorption. The present study showed that cattail and water hyacinth biomass are promising biosorbents that provide a green, practical, and cheap solution to household water filtering systems in rural communities

Gene transfer across species boundaries in bryophytes : evidence from major life cycle stages in Homalothecium lutescens and H. sericeum

Background and Aims: The mosses Homalothecium lutescens and H. sericeum are genetically, morphologically and ecologically differentiated; mixed populations sometimes occur. In sympatric populations, intermediate character states among gametophytes and sporophytes have been observed, suggesting hybridization and introgression in such populations. Methods: We determined genotypes using bi-allelic co-dominant single nucleotide polymorphism (SNP) markers, specific to either H. lutescens or H. sericeum, to estimate the degree of genetic mixing in 449 moss samples collected from seven sympatric and five allopatric populations on the island of Öland, south Sweden. The samples represented three generations: haploid maternal gametophytes; diploid sporophytes; and haploid sporelings. Key Results: Admixture analyses of SNP genotypes identified a majority as pure H. lutescens or H. sericeum, but 76 samples were identified as mildly admixed (17 %) and 17 samples (3.8 %) as strongly admixed. Admixed samples were represented in all three generations in several populations. Hybridization and introgression were bidirectional. Conclusions: Our results demonstrate that admixed genomes are transferred between the generations, so that the populations behave as true hybrid zones. Earlier studies of sympatric bryophyte populations with admixed individuals have not been able to show that admixed alleles are transferred beyond the first generation. The presence of true hybrid zones has strong evolutionary implications because genetic material transferred across species boundaries can be directly exposed to selection in the long-lived haploid generation of the bryophyte life cycle, and contribute to local adaptation, long-term survival and speciation

Evolutionary History of the Marchantia polymorpha Complex

The potential role of introgression in evolution has gained increased interest in recent years. Although some fascinating examples have been reported, more information is needed to generalize the importance of hybridization and introgression for adaptive divergence. As limited data exist on haploid dominant species, we analyzed genomes of three subspecies of the liverwortMarchantia polymorpha. We used available genomic data for subsp.ruderalisand carried out whole-genome (PacBio) sequencing for one individual each of subsp.montivagansand subsp.polymorphaas well as Illumina resequencing of additional genomes for all three subspecies. The three subspecies were compared againstM. paleaceaas outgroup. Our analyses revealed separation of the three taxa, but all three possible topologies were richly represented across the genomes, and the underlying divergence order less obvious. This uncertainty could be the result of the divergence of the three subspecies close in time, or that introgression has been frequent since divergence. In particular, we found that pseudo-chromosome 2 in subsp.montivaganswas much more diverged than other parts of the genomes. This could either be explained by specific capture of chromosome 2 from an unknown related species through hybridization or by conservation of chromosome 2 despite intermittent or ongoing introgression affecting more permeable parts of the genomes. A higher degree of chromosomal rearrangements on pseudo-chromosome 2 support the second hypothesis. Species tree analyses recovered an overall topology where subsp.montivagansdiverged first and subsp.ruderalisand subsp.polymorphaappeared as sister lineages. Each subspecies was associated with its own chloroplast and mitochondrial haplotype group. Our data suggest introgression but refute a previous hypothesis that subsp.ruderalisis a new stabilized hybrid between the other two subspecies

Comparative Toxicity of Heavy Metals Cd, Pb, and Zn to Three Acrocarpous Moss Species using Chlorophyll Contents

Mosses have often been used for biomonitoring because of their diversity of habitats, structural simplicity, and rapid multiplication rate. This research aimed to study the tolerance of heavy metal in 3 species of terricolous mosses i.e., Barbula consanguinea, Hyophila apiculata, and H. involuta. The gametophores of mosses were immersed at 4 concentrations of each of the heavy metals Cd, Pb, and Zn as well as in controls with no heavy metal. After 10, 20, and 30 days of exposure, mosses were extracted for chlorophyll-a in ethanol. The extracted chlorophyll-a was analyzed by spectrophotometer at 664 nm. The results revealed that the amount of chlorophyll-a in all species decreased with increasing concentrations of Cd, Pb, and Zn. The degree of metal toxicity for all species was Cd > Pb > Zn. By comparing the ratio of extracted chlorophyll-a in heavy metal-treated mosses to chlorophyll-a extracted in control mosses, the tolerance against 3 heavy metals in 3 mosses was H. involuta > B. consanguinea > H. apiculata. Possibly, H. involuta can be used for biomonitoring of heavy metals in contaminated environments in the future