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1.  Effects of Essential Oils from Eucalyptus globulus Leaves on Soil Organisms Involved in Leaf Degradation 
PLoS ONE  2013;8(4):e61233.
The replacement of native Portuguese forests by Eucalyptus globulus is often associated with deleterious effects on terrestrial and aquatic communities. Several studies have suggested that such a phenomenon is linked with the leaf essential oils released into the environment during the Eucalyptus leaf degradation process. However, to date, the way these compounds affect leaf degradation in terrestrial systems i.e. by direct toxic effects to soil invertebrates or indirectly by affecting food of soil fauna, is still unknown. In order to explore this question, the effect of essential oils extracted from E. globulus leaves on terrestrial systems was investigated. Fungal growth tests with species known as leaf colonizers (Mucor hiemalis, Alternaria alternata, Penicillium sp., Penicillium glabrum and Fusarium roseum) were performed to evaluate the antifungal effect of essential oils. In addition, a reproduction test with the collembolans Folsomia candida was done using a gradient of eucalyptus essential oils in artificial soil. The influence of essential oils on feeding behaviour of F. candida and the isopods Porcellio dilatatus was also investigated through food avoidance and consumption tests. Eucalyptus essential oils were lethal at concentrations between 2.5–20 µL/mL and inhibited growth of all fungal species between 1.25–5 µL/mL. The collembolan reproduction EC50 value was 35.0 (28.6–41.2) mg/kg and both collembola and isopods preferred leaves without oils. Results suggested that the effect of essential oils in leaf processing is related to direct toxic effects on fungi and soil fauna and to indirect effects on the quality and availability of food to soil invertebrates.
PMCID: PMC3618273  PMID: 23577212
2.  Reproductive Flexibility: Genetic Variation, Genetic Costs and Long-Term Evolution in a Collembola 
PLoS ONE  2008;3(9):e3207.
In a variable yet predictable world, organisms may use environmental cues to make adaptive adjustments to their phenotype. Such phenotypic flexibility is expected commonly to evolve in life history traits, which are closely tied to Darwinian fitness. Yet adaptive life history flexibility remains poorly documented. Here we introduce the collembolan Folsomia candida, a soil-dweller, parthenogenetic (all-female) microarthropod, as a model organism to study the phenotypic expression, genetic variation, fitness consequences and long-term evolution of life history flexibility. We demonstrate that collembola have a remarkable adaptive ability for adjusting their reproductive phenotype: when transferred from harsh to good conditions (in terms of food ration and crowding), a mother can fine-tune the number and the size of her eggs from one clutch to the next. The comparative analysis of eleven clonal populations of worldwide origins reveals (i) genetic variation in mean egg size under both good and bad conditions; (ii) no genetic variation in egg size flexibility, consistent with convergent evolution to a common physiological limit; (iii) genetic variation of both mean reproductive investment and reproductive investment flexibility, associated with a reversal of the genetic correlation between egg size and clutch size between environmental conditions ; (iv) a negative genetic correlation between reproductive investment flexibility and adult lifespan. Phylogenetic reconstruction shows that two life history strategies, called HIFLEX and LOFLEX, evolved early in evolutionary history. HIFLEX includes six of our 11 clones, and is characterized by large mean egg size and reproductive investment, high reproductive investment flexibility, and low adult survival. LOFLEX (the other five clones) has small mean egg size and low reproductive investment, low reproductive investment flexibility, and high adult survival. The divergence of HIFLEX and LOFLEX could represent different adaptations to environments differing in mean quality and variability, or indicate that a genetic polymorphism of reproductive investment reaction norms has evolved under a physiological tradeoff between reproductive investment flexibility and adult lifespan.
PMCID: PMC2527682  PMID: 18791644
3.  Fitness consequences of maternal and grandmaternal effects 
Ecology and Evolution  2014;4(15):3139-3145.
Transgenerational effects are broader than only parental relationships. Despite mounting evidence that multigenerational effects alter phenotypic and life-history traits, our understanding of how they combine to determine fitness is not well developed because of the added complexity necessary to study them. Here, we derive a quantitative genetic model of adaptation to an extraordinary new environment by an additive genetic component, phenotypic plasticity, maternal and grandmaternal effects. We show how, at equilibrium, negative maternal and negative grandmaternal effects maximize expected population mean fitness. We define negative transgenerational effects as those that have a negative effect on trait expression in the subsequent generation, that is, they slow, or potentially reverse, the expected evolutionary dynamic. When maternal effects are positive, negative grandmaternal effects are preferred. As expected under Mendelian inheritance, the grandmaternal effects have a lower impact on fitness than the maternal effects, but this dual inheritance model predicts a more complex relationship between maternal and grandmaternal effects to constrain phenotypic variance and so maximize expected population mean fitness in the offspring.
PMCID: PMC4161186  PMID: 25247070
Adaptation; indirect genetic effect; maternal effect; phenotypic evolution; phenotypic plasticity; quantitative genetics
4.  Effects of ecological flooding on the temporal and spatial dynamics of carabid beetles (Coleoptera, Carabidae) and springtails (Collembola) in a polder habitat 
ZooKeys  2011;421-446.
Within the scope of the Integrated Rhine Program an ecological flood gate and channel was inserted into the polder “Ingelheim” to enhance animal and plant diversity. In 2008, carabid beetles and springtails were collected, using pitfall traps, to measure the effects of ecological flooding and a strong precipitation event at a flood-disturbed and a dry location in this area. At both localities, xerophilic and mesophilic carabid beetle species were dominant throughout the study period. The total number of individuals of hygrophilic species was comparatively constant, while species number increased, partly due to the changed moisture conditions caused by ecological flooding and strong precipitation. Carabid beetle diversity and evenness decreased marginally when ecological flooding was absent. Springtails represent a less mobile arthropod order, and as such the impact of ecological flooding was stronger. An increase in both numbers of species and individuals of hygrophilic and hygrotolerant species occurred in the flood-disturbed location after ecological flooding. After the sites at both locations had dried, the number of individuals belonging to these species declined rapidly. In contrast to carabid species, the strong precipitation event showed no influence on hygrophilic springtail species. Thus, collembolan diversity and evenness decreased markedly in the absence of flooding. We showed that ecological flooding has an influence on the spatial and temporal dynamics of different arthropod groups that inhabit the polder “Ingelheim”. These findings demonstrate the importance of using different arthropod groups as bioindicators in determining the ecological value of a particular polder design.
PMCID: PMC3131029  PMID: 21738425
bioindication; community dynamics; drought; flooding; Integrated Rhine Program (IRP)
5.  New Method for Automatic Body Length Measurement of the Collembolan, Folsomia candida Willem 1902 (Insecta: Collembola) 
PLoS ONE  2014;9(6):e98230.
The collembolan, Folsomia candida, is widely used in soil ecotoxicology. In recent years, growth rate of collembolans has become as frequently used endpoint as reproduction rate in ecotoxicological studies. However, measuring collembolan body sizes to estimate growth rate is a complicated and time-consuming task. Here we present a new image analysis method, which facilitates and accelerates the body length measurement of the collembolan Folsomia candida. The new software package, called CollScope, consists of three elements: 1) an imaging device; 2) photographing software; 3) an ImageJ macro for image processing, measurement and data analysis. We give a complete description of the operation of the software, the image analyzing process and describe its accuracy and reliability. The software with a detailed usage manual is attached as Supplementary Material. We report a case study to demonstrate that the automated measurement of collembolan body sizes is highly correlated with the traditional manual measurements (estimated measuring accuracy 0.05 mm). Furthermore, we performed a dose-response ecotoxicity test using cadmium-sulfate by using CollScope as well as classical methods for size measurement. Size data measured by CollScope or manually did not differ significantly. Furthermore the new software package decreased time consumption of the measurements to 42% when tested on 35 animals. Consequently, methodological investigations performed in this study should be regarded as a recommendation for any other routine dose-response study where body growth is an endpoint.
PMCID: PMC4046991  PMID: 24901322
6.  The complete mitochondrial genome of the Antarctic springtail Cryptopygus antarcticus (Hexapoda: Collembola) 
BMC Genomics  2008;9:315.
Mitogenomics data, i.e. complete mitochondrial genome sequences, are popular molecular markers used for phylogenetic, phylogeographic and ecological studies in different animal lineages. Their comparative analysis has been used to shed light on the evolutionary history of given taxa and on the molecular processes that regulate the evolution of the mitochondrial genome. A considerable literature is available in the fields of invertebrate biochemical and ecophysiological adaptation to extreme environmental conditions, exemplified by those of the Antarctic. Nevertheless, limited molecular data are available from terrestrial Antarctic species, and this study represents the first attempt towards the description of a mitochondrial genome from one of the most widespread and common collembolan species of Antarctica.
In this study we describe the mitochondrial genome of the Antarctic collembolan Cryptopygus antarcticus Willem, 1901. The genome contains the standard set of 37 genes usually present in animal mtDNAs and a large non-coding fragment putatively corresponding to the region (A+T-rich) responsible for the control of replication and transcription. All genes are arranged in the gene order typical of Pancrustacea. Three additional short non-coding regions are present at gene junctions. Two of these are located in positions of abrupt shift of the coding polarity of genes oriented on opposite strands suggesting a role in the attenuation of the polycistronic mRNA transcription(s). In addition, remnants of an additional copy of trnL(uag) are present between trnS(uga) and nad1. Nucleotide composition is biased towards a high A% and T% (A+T = 70.9%), as typically found in hexapod mtDNAs. There is also a significant strand asymmetry, with the J-strand being more abundant in A and C. Within the A+T-rich region, some short sequence fragments appear to be similar (in position and primary sequence) to those involved in the origin of the N-strand replication of the Drosophila mtDNA.
The mitochondrial genome of C. antarcticus shares several features with other pancrustacean genomes, although the presence of unusual non-coding regions is also suggestive of molecular rearrangements that probably occurred before the differentiation of major collembolan families. Closer examination of gene boundaries also confirms previous observations on the presence of unusual start and stop codons, and suggests a role for tRNA secondary structures as potential cleavage signals involved in the maturation of the primary transcript. Sequences potentially involved in the regulation of replication/transcription are present both in the A+T-rich region and in other areas of the genome. Their position is similar to that observed in a limited number of insect species, suggesting unique replication/transcription mechanisms for basal and derived hexapod lineages. This initial description and characterization of the mitochondrial genome of C. antarcticus will constitute the essential foundation prerequisite for investigations of the evolutionary history of one of the most speciose collembolan genera present in Antarctica and other localities of the Southern Hemisphere.
PMCID: PMC2483729  PMID: 18593463
7.  Selective foraging of fungi by collembolans in soil 
Biology Letters  2005;1(2):243-246.
Soils contain highly diverse communities of microorganisms and invertebrates. The trophic interactions between these species are largely unknown. Collembolans form an abundant part of the invertebrate community in soils. A prevailing view is that soil collembolans are generalist feeders on fungi, lichens, fragmented litter and bacteria. However, in laboratory food choice experiments, it has been shown that collembolans preferentially select certain taxa of fungi. To examine this apparent contradiction, we developed a molecular technique based on the analysis of 18S ribosomal DNA (rDNA) sequences to explore the diversity of fungi in soils and in the guts of collembolans. We report that the diversity of fungi found in the natural soil was 33 times higher than that in the guts of the collembolan Protaphorura armata. The data support the view that collembolan species can be highly selective when foraging on fungi in soils.
PMCID: PMC1626218  PMID: 17148177
collembolan; food selection; soil food web; ribosomal DNA; fungi
8.  Phototactic Responses to Ultraviolet and White Light in Various Species of Collembola, Including the Eyeless Species, Folsomia candida  
Previous observations have indicated homology in the cellular components between collembolan eyes and the compound eyes of insects. However, behavioral or physiological studies indicating similarities in function are lacking. Collembolan eyes were examined from three species in the Family Isotomidae using scanning electron microscopy. Collembolan eyes are arranged dorsally and laterally on each side of the head in two species, Proisotoma minuta with eight eyes on each side of the head and Folsomia similis with one eye on each side of the head. In both of these species the eyes were located just posterior to the postantennal organ. In Folsomia candida, no external eye structures were detected. These three species were assayed for a series of behavioral preferences using ultraviolet (UV), white light and dark, and temperature conditions. The tests demonstrated that over 76% of all three species, including the eyeless F. Candida, chose white over UV light, over 69% preferred dark over UV, and over 77% favored dark over white light. The results demonstrated that all three species detect both UV and white light and avoid it, preferring cool, dark habitats. From the results of this study, it is hypothesized that F. candida may, in fact, be only “lensless” and may be able to detect light by having internal, non-ocular photoreceptors. Further histological studies are needed to investigate this possibility.
PMCID: PMC2999417  PMID: 20307231
Isotomidae; photoreceptors; SEM; ommatidium; behavior
9.  Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment. 
Emergence from an aquatic environment to the land is one of the major evolutionary transitions within the arthropods. It is often considered that the first hexapods, and in particular the first springtails, were semi-aquatic and this assumption drives evolutionary models towards particular conclusions. To address the question of the ecological origin of the springtails, phylogenetic analyses by optimization alignment were performed on D1 and D2 regions of the 28S rDNA for 55 collembolan exemplars and eight outgroups. Relationships among the orders Symphypleona, Entomobryomorpha and Poduromorpha are inferred. More specifically, a robust hypothesis is provided for the subfamilial relationships within the order Poduromorpha. Contrary to previous statements, the semi-aquatic species Podura aquatica is not basal or 'primitive', but well nested in the Poduromorpha. The analyses performed for the 24 different weighting schemes yielded the same conclusion: semi-aquatic ecology is not ancestral for the springtails. It is a derived condition that evolved independently several times. The adaptation for semi-aquatic life is better interpreted as a step towards independence from land, rather than indication of an aquatic origin.
PMCID: PMC1691003  PMID: 12061958
10.  The effect of autocorrelation in environmental variability on the persistence of populations: an experimental test. 
Despite its significance regarding the conservation and management of biological resources, the body of theory predicting that the correlation between successive environmental states can profoundly influence extinction has not been empirically validated. Identical clonal populations from a model experimental system based on the collembolan Folsomia candida were used in the present study to investigate the effect of environmental autocorrelation on time to extinction. Environmental variation was imposed by variable implementation (present/absent) of a culling procedure according to treatments that represented six patterns of environmental autocorrelation. The average number of culling events was held constant across treatments but, as environmental autocorrelation increased, longer runs of both favourable and unfavourable culling tended to occur. While no difference was found among the survival functions for the various treatments, the time taken for 50% of the component populations to become extinct decreased significantly with increasing environmental autocorrelation. Similarly, analysis of all extinct populations demonstrated that time to extinction was shortened as environmental autocorrelation increased. However, this acceleration of extinction can be fully offset if sequential introduction is used in place of simultaneous introduction when founding the populations.
PMCID: PMC1691845  PMID: 15475334
11.  Collembase: a repository for springtail genomics and soil quality assessment 
BMC Genomics  2007;8:341.
Environmental quality assessment is traditionally based on responses of reproduction and survival of indicator organisms. For soil assessment the springtail Folsomia candida (Collembola) is an accepted standard test organism. We argue that environmental quality assessment using gene expression profiles of indicator organisms exposed to test substrates is more sensitive, more toxicant specific and significantly faster than current risk assessment methods. To apply this species as a genomic model for soil quality testing we conducted an EST sequencing project and developed an online database.
Collembase is a web-accessible database comprising springtail (F. candida) genomic data. Presently, the database contains information on 8686 ESTs that are assembled into 5952 unique gene objects. Of those gene objects ~40% showed homology to other protein sequences available in GenBank (blastx analysis; non-redundant (nr) database; expect-value < 10-5). Software was applied to infer protein sequences. The putative peptides, which had an average length of 115 amino-acids (ranging between 23 and 440) were annotated with Gene Ontology (GO) terms. In total 1025 peptides (~17% of the gene objects) were assigned at least one GO term (expect-value < 10-25). Within Collembase searches can be conducted based on BLAST and GO annotation, cluster name or using a BLAST server. The system furthermore enables easy sequence retrieval for functional genomic and Quantitative-PCR experiments. Sequences are submitted to GenBank (Accession numbers: EV473060 – EV481745).
Collembase is a resource of sequence data on the springtail F. candida. The information within the database will be linked to a custom made microarray, based on the Agilent platform, which can be applied for soil quality testing. In addition, Collembase supplies information that is valuable for related scientific disciplines such as molecular ecology, ecogenomics, molecular evolution and phylogenetics.
PMCID: PMC2234260  PMID: 17900339
12.  Transcriptomics reveals extensive inducible biotransformation in the soil-dwelling invertebrate Folsomia candida exposed to phenanthrene 
BMC Genomics  2009;10:236.
Polycyclic aromatic hydrocarbons are common pollutants in soil, have negative effects on soil ecosystems, and are potentially carcinogenic. The Springtail (Collembola) Folsomia candida is often used as an indicator species for soil toxicity. Here we report a toxicogenomic study that translates the ecological effects of the polycyclic aromatic hydrocarbon phenanthrene in soil to the early transcriptomic responses in Folsomia candida.
Microarrays were used to examine two different exposure concentrations of phenanthrene, namely the EC10 (24.95 mg kg-1 soil) and EC50 (45.80 mg kg-1 soil) on reproduction of this springtail, which evoked 405 and 251 differentially expressed transcripts, respectively. Fifty transcripts were differential in response to either concentration. Many transcripts encoding xenobiotic detoxification and biotransformation enzymes (phases I, II, and III) were upregulated in response to either concentration. Furthermore, indications of general and oxidative stress were found in response to phenanthrene. Chitin metabolism appeared to be disrupted particularly at the low concentration, and protein translation appeared suppressed at the high concentration of phenanthrene; most likely in order to reallocate energy budgets for the detoxification process. Finally, an immune response was evoked especially in response to the high effect concentration, which was also described in a previous transcriptomic study using the same effect concentration (EC50) of cadmium.
Our study provides new insights in the molecular mode of action of the important polluting class of polycyclic aromatic hydrocarbons in soil animals. Furthermore, we present a fast, sensitive, and specific soil toxicity test which enhances traditional tests and may help to improve current environmental risk assessments and monitoring of potentially polluted sites.
PMCID: PMC2688526  PMID: 19457238
13.  Transgenerational effects and the cost of ant tending in aphids 
Oecologia  2013;173(3):779-790.
In mutualistic interactions, partners obtain a net benefit, but there may also be costs associated with the provision of benefits for a partner. The question of whether aphids suffer such costs when attended by ants has been raised in previous work. Transgenerational effects, where offspring phenotypes are adjusted based on maternal influences, could be important in the mutualistic interaction between aphids and ants, in particular because aphids have telescoping generations where two offspring generations can be present in a mature aphid. We investigated the immediate and transgenerational influence of ant tending on aphid life history and reproduction by observing the interaction between the facultative myrmecophile Aphis fabae and the ant Lasius niger over 13 aphid generations in the laboratory. We found that the effect of ant tending changes dynamically over successive aphid generations after the start of tending. Initially, total aphid colony weight, aphid adult weight and aphid embryo size decreased compared with untended aphids, consistent with a cost of ant association, but these differences disappeared within four generations of interaction. We conclude that transgenerational effects are important in the aphid–ant interactions and that the costs for aphids of being tended by ants can vary over generations.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-013-2659-y) contains supplementary material, which is available to authorized users.
PMCID: PMC3825118  PMID: 23689730
Aphid–ant mutualism; Maternal effects; Reproductive investment; Embryo size; Plasticity
14.  Habitat structure alters top-down control in litter communities 
Oecologia  2012;172(3):877-887.
The question whether top-down or bottom-up forces dominate trophic relationships, energy flow, and abundances within food webs has fuelled much ecological research with particular focus on soil litter ecosystems. Because litter simultaneously provides habitat structure and a basal resource, disentangling direct trophic and indirect non-trophic effects on different trophic levels remains challenging. Here, we focussed on short-term per capita interaction strengths of generalist predators (centipedes) on their microbi-detritivore prey (springtails) and addressed how the habitat structuring effects of the leaf litter modifies this interaction. We performed a series of laboratory functional response experiments where four levels of habitat structure were constructed by adding different amounts of leaf litter to the experimental arenas. We found that increased leaf litter reduced the consumption rate of the predator. We interpreted this as a dilution effect of the augmented habitat size provided by the increasing leaf litter surface available to the species. Dilution of the prey population decreased encounter rates, whereas the capture success was not affected. Interestingly, our results imply that top-down control by centipedes decreased with increasing resource supply for the microbi-detritivore prey (i.e. the leaf litter that simultaneously provides habitat structure). Therefore, effective top-down control of predators on microbi-detritvore populations seems unlikely in litter-rich ecosystems due to the non-trophic, habitat-structuring effect of the basal litter resource.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-012-2530-6) contains supplementary material, which is available to authorized users.
PMCID: PMC3679420  PMID: 23188055
Bottom-up control; Functional response; Non-linear interaction strength; Predator–prey interaction; Soil food webs
15.  Tree Species Traits Influence Soil Physical, Chemical, and Biological Properties in High Elevation Forests 
PLoS ONE  2009;4(6):e5964.
Previous studies have shown that plants often have species-specific effects on soil properties. In high elevation forests in the Southern Rocky Mountains, North America, areas that are dominated by a single tree species are often adjacent to areas dominated by another tree species. Here, we assessed soil properties beneath adjacent stands of trembling aspen, lodgepole pine, and Engelmann spruce, which are dominant tree species in this region and are distributed widely in North America. We hypothesized that soil properties would differ among stands dominated by different tree species and expected that aspen stands would have higher soil temperatures due to their open structure, which, combined with higher quality litter, would result in increased soil respiration rates, nitrogen availability, and microbial biomass, and differences in soil faunal community composition.
Methodology/Principal Findings
We assessed soil physical, chemical, and biological properties at four sites where stands of aspen, pine, and spruce occurred in close proximity to one-another in the San Juan Mountains, Colorado. Leaf litter quality differed among the tree species, with the highest nitrogen (N) concentration and lowest lignin∶N in aspen litter. Nitrogen concentration was similar in pine and spruce litter, but lignin∶N was highest in pine litter. Soil temperature and moisture were highest in aspen stands, which, in combination with higher litter quality, probably contributed to faster soil respiration rates from stands of aspen. Soil carbon and N content, ammonium concentration, and microbial biomass did not differ among tree species, but nitrate concentration was highest in aspen soil and lowest in spruce soil. In addition, soil fungal, bacterial, and nematode community composition and rotifer, collembolan, and mesostigmatid mite abundance differed among the tree species, while the total abundance of nematodes, tardigrades, oribatid mites, and prostigmatid mites did not.
Although some soil characteristics were unaffected by tree species identity, our results clearly demonstrate that these dominant tree species are associated with soils that differ in several physical, chemical, and biotic properties. Ongoing environmental changes in this region, e.g. changes in fire regime, frequency of insect outbreaks, changes in precipitation patterns and snowpack, and land-use change, may alter the relative abundance of these tree species over coming decades, which in turn will likely alter the soils.
PMCID: PMC2694365  PMID: 19536334
16.  Molecular evolution of the crustacean hyperglycemic hormone family in ecdysozoans 
Crustacean Hyperglycemic Hormone (CHH) family peptides are neurohormones known to regulate several important functions in decapod crustaceans such as ionic and energetic metabolism, molting and reproduction. The structural conservation of these peptides, together with the variety of functions they display, led us to investigate their evolutionary history. CHH family peptides exist in insects (Ion Transport Peptides) and may be present in all ecdysozoans as well. In order to extend the evolutionary study to the entire family, CHH family peptides were thus searched in taxa outside decapods, where they have been, to date, poorly investigated.
CHH family peptides were characterized by molecular cloning in a branchiopod crustacean, Daphnia magna, and in a collembolan, Folsomia candida. Genes encoding such peptides were also rebuilt in silico from genomic sequences of another branchiopod, a chelicerate and two nematodes. These sequences were included in updated datasets to build phylogenies of the CHH family in pancrustaceans. These phylogenies suggest that peptides found in Branchiopoda and Collembola are more closely related to insect ITPs than to crustacean CHHs. Datasets were also used to support a phylogenetic hypothesis about pancrustacean relationships, which, in addition to gene structures, allowed us to propose two evolutionary scenarios of this multigenic family in ecdysozoans.
Evolutionary scenarios suggest that CHH family genes of ecdysozoans originate from an ancestral two-exon gene, and genes of arthropods from a three-exon one. In malacostracans, the evolution of the CHH family has involved several duplication, insertion or deletion events, leading to neuropeptides with a wide variety of functions, as observed in decapods. This family could thus constitute a promising model to investigate the links between gene duplications and functional divergence.
PMCID: PMC2841656  PMID: 20184761
17.  Secondary chemicals protect mould from fungivory 
Biology Letters  2007;3(5):523-525.
The vast repertoire of toxic fungal secondary metabolites has long been assumed to have an evolved protective role against fungivory. It still remains elusive, however, whether fungi contain these compounds as an anti-predator adaptation. We demonstrate that loss of secondary metabolites in the soil mould Aspergillus nidulans causes, under the attack of the fungivorous springtail Folsomia candida, a disadvantage to the fungus. Springtails exhibited a distinct preference for feeding on a mutant deleted for LaeA, a global regulator of Aspergillus secondary metabolites. Consumption of the mutant yielded a reproductive advantage to the arthropod but detrimental effects on fungal biomass compared with a wild-type fungus capable of producing the entire arsenal of secondary metabolites. Our results demonstrate that fungal secondary metabolites shape food choice behaviour, can affect population dynamics of fungivores, and suggest that fungivores may provide a selective force favouring secondary metabolites synthesis in fungi.
PMCID: PMC2391202  PMID: 17686752
chemical defence; filamentous fungi; food choice; LaeA; secondary metabolites; soil arthropods
18.  Transgenerational acclimation of fishes to climate change and ocean acidification 
F1000Prime Reports  2014;6:99.
There is growing concern about the impacts of climate change and ocean acidification on marine organisms and ecosystems, yet the potential for acclimation and adaptation to these threats is poorly understood. Whereas many short-term experiments report negative biological effects of ocean warming and acidification, new studies show that some marine species have the capacity to acclimate to warmer and more acidic environments across generations. Consequently, transgenerational plasticity may be a powerful mechanism by which populations of some species will be able to adjust to projected climate change. Here, I review recent advances in understanding transgenerational acclimation in fishes. Research over the past 2 to 3 years shows that transgenerational acclimation can partially or fully ameliorate negative effects of warming, acidification, and hypoxia in a range of different species. The molecular and cellular pathways underpinning transgenerational acclimation are currently unknown, but modern genetic methods provide the tools to explore these mechanisms. Despite the potential benefits of transgenerational acclimation, there could be limitations to the phenotypic traits that respond transgenerationally, and trade-offs between life stages, that need to be investigated. Future studies should also test the potential interactions between transgenerational plasticity and genetic evolution to determine how these two processes will shape adaptive responses to environmental change over coming decades.
PMCID: PMC4229724  PMID: 25580253
19.  Cadmium affects toxicokinetics of pyrene in the collembolan Folsomia candida 
Ecotoxicology (London, England)  2012;21(3):795-802.
Since toxicity is time dependent, short-term toxicity tests may overlook mixture effects, because chemical accumulation within an organism takes time. We therefore studied the effects of cadmium on the toxicokinetics of pyrene and its metabolites in the soil-dwelling collembolan Folsomia candida exposed through Lufa 2.2 soil. Single pyrene was rapidly taken up and steady state was reached within the 337-h exposure period. Simultaneous exposure to cadmium significantly decreased the pyrene uptake and elimination rate, resulting in a prolonged half life. Kinetics of the first phase metabolite OH-pyrene was also significantly influenced by cadmium. Cadmium increased the hydroxylation rate of pyrene but slowed down its further metabolization, again resulting in a prolonged half life. We showed that pyrene accumulation and metabolization are significantly influenced by the presence of cadmium. Our results suggest that mixture effects may be dependent on exposure time.
PMCID: PMC3310129  PMID: 22327388
Uptake and elimination kinetics; Polycyclic aromatic hydrocarbons; Biotransformation; Soil arthropods; Mixtures
20.  Antibiotic treatment leads to the elimination of Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia candida 
BMC Biology  2009;7:54.
Wolbachia is an extremely widespread bacterial endosymbiont of arthropods and nematodes that causes a variety of reproductive peculiarities. Parthenogenesis is one such peculiarity but it has been hypothesised that this phenomenon may be functionally restricted to organisms that employ haplodiploid sex determination. Using two antibiotics, tetracycline and rifampicin, we attempted to eliminate Wolbachia from the diplodiploid host Folsomia candida, a species of springtail which is a widely used study organism.
Molecular assays confirmed that elimination of Wolbachia was successfully achieved through continuous exposure of populations (over two generations and several weeks) to rifampicin administered as 2.7% dry weight of their yeast food source. The consequence of this elimination was total sterility of all individuals, despite the continuation of normal egg production.
Microbial endosymbionts play an obligatory role in the reproduction of their diplodiploid host, most likely one in which the parthenogenetic process is facilitated by Wolbachia. A hitherto unknown level of host-parasite interdependence is thus recorded.
PMCID: PMC2739161  PMID: 19698188
21.  Change in paternal grandmothers´ early food supply influenced cardiovascular mortality of the female grandchildren 
BMC Genetics  2014;15:12.
This study investigated whether large fluctuations in food availability during grandparents' early development influenced grandchildren's cardiovascular mortality. We reported earlier that changes in availability of food - from good to poor or from poor to good - during intrauterine development was followed by a double risk of sudden death as an adult, and that mortality rate can be associated with ancestors´ childhood availability of food. We have now studied transgenerational responses (TGR) to sharp differences of harvest between two consecutive years´ for ancestors of 317 people in Överkalix, Sweden.
The confidence intervals were very wide but we found a striking TGR. There was no response in cardiovascular mortality in the grandchild from sharp changes of early exposure, experienced by three of the four grandparents (maternal grandparents and paternal grandfathers). If, however, the paternal grandmother up to puberty lived through a sharp change in food supply from one year to next, her sons´ daughters had an excess risk for cardiovascular mortality (HR 2.69, 95% confidence interval 1.05-6.92). Selection or learning and imitation are unlikely explanations. X-linked epigenetic inheritance via spermatozoa seemed to be plausible, with the transmission, limited to being through the father, possibly explained by the sex differences in meiosis.
The shock of change in food availability seems to give specific transgenerational responses.
PMCID: PMC3929550  PMID: 24552514
Epidemiology; Food change; Environmental shock; Human transgenerational response; Cardiovascular mortality; Överkalix
22.  Diet alters delayed selfing, inbreeding depression, and reproductive senescence in a freshwater snail 
Ecology and Evolution  2014;4(14):2968-2977.
Reproductive success is a critical fitness attribute that is directly influenced by resource availability. Here, we investigate the effects of diet-based resource availability on three interrelated aspects of reproductive success: a change in mating system based on mate availability, consequent inbreeding depression, and the deterioration of reproductive efficiency with age (senescence). We employed a factorial experimental design using 22 full-sib families of the hermaphroditic freshwater snail Physa acuta to explore these interactions. Individual snails were reared in one of two mate-availability treatments (isolated [selfing] or occasionally paired [outcrossing]) and one of two diet treatments (boiled lettuce or Spirulina, an algae that is rich in protein, vitamins, and minerals). Spirulina-fed snails initiated reproduction at a 13% earlier age and 7% larger size than lettuce-fed snails. Spirulina also resulted in a 30% reduction in the time delay before selfing. Compared to lettuce, a diet of Spirulina increased inbreeding depression by 52% for egg hatching rate and 64% for posthatching juvenile survival. Furthermore, Spirulina led to a 15-fold increase in the rate of reproductive senescence compared with a diet of lettuce. These transgenerational, interactive effects of diet on inbreeding depression and reproductive senescence are discussed in the context of diet-induced phenotypic plasticity.
PMCID: PMC4130452  PMID: 25165532
Age at first reproduction; aging; caloric restriction; mating system; pulmonate; transgenerational effects; waiting time
23.  QTL architecture of reproductive fitness characters in Brassica rapa 
BMC Plant Biology  2014;14:66.
Reproductive output is critical to both agronomists seeking to increase seed yield and to evolutionary biologists interested in understanding natural selection. We examine the genetic architecture of diverse reproductive fitness traits in recombinant inbred lines (RILs) developed from a crop (seed oil) × wild-like (rapid cycling) genotype of Brassica rapa in field and greenhouse environments.
Several fitness traits showed strong correlations and QTL-colocalization across environments (days to bolting, fruit length and seed color). Total fruit number was uncorrelated across environments and most QTL affecting this trait were correspondingly environment-specific. Most fitness components were positively correlated, consistent with life-history theory that genotypic variation in resource acquisition masks tradeoffs. Finally, we detected evidence of transgenerational pleiotropy, that is, maternal days to bolting was negatively correlated with days to offspring germination. A QTL for this transgenerational correlation was mapped to a genomic region harboring one copy of FLOWERING LOCUS C, a genetic locus known to affect both days to flowering as well as germination phenotypes.
This study characterizes the genetic structure of important fitness/yield traits within and between generations in B. rapa. Several identified QTL are suitable candidates for fine-mapping for the improvement of yield in crop Brassicas. Specifically, brFLC1, warrants further investigation as a potential regulator of phenology between generations.
PMCID: PMC4004417  PMID: 24641198
Fitness components; Life-history traits; Phenotypic plasticity; Transgenerational effects; Yield; Brassica rapa
24.  Detection of Transgenerational Spermatogenic Inheritance of Adult Male Acquired CNS Gene Expression Characteristics Using a Drosophila Systems Model 
PLoS ONE  2009;4(6):e5763.
Available instances of inheritance of epigenetic transgenerational phenotype are limited to environmental exposures during embryonic and adult gonadal development. Adult exposures can also affect gametogenesis and thereby potentially result in reprogramming of the germline. Although examples of epigenetic effects on gametogenesis exist, it is notable that transgenerational inheritance of environment-induced adult phenotype has not yet been reported. Epigenetic codes are considered to be critical in neural plasticity. A Drosophila systems model of pentylenetetrazole (PTZ) induced long-term brain plasticity has recently been described. In this model, chronic PTZ treatment of adult males causes alterations in CNS transcriptome. Here, we describe our search for transgenerational spermatogenic inheritance of PTZ induced gene expression phenotype acquired by adult Drosophila males. We generated CNS transcriptomic profiles of F1 adults after treating F0 adult males with PTZ and of F2 adults resulting from a cross between F1 males and normal females. Surprisingly, microarray clustering showed F1 male profile as closest to F1 female and F0 male profile closest to F2 male. Differentially expressed genes in F1 males, F1 females and F2 males showed significant overlap with those caused by PTZ. Interestingly, microarray evidence also led to the identification of upregulated rRNA in F2 males. Next, we generated microarray expression profiles of adult testis from F0 and F1 males. Further surprising, clustering of CNS and testis profiles and matching of differentially expressed genes in them provided evidence of a spermatogenic mechanism in the transgenerational effect observed. To our knowledge, we report for the first time detection of transgenerational spermatogenic inheritance of adult acquired somatic gene expression characteristic. The Drosophila systems model offers an excellent opportunity to understand the epigenetic mechanisms underlying the phenomenon. The finding that adult acquired transcriptomic alteration in soma is spermatogenically inherited across generations has potential implications in human health and evolution.
PMCID: PMC2685453  PMID: 19503609
25.  Smart Skin Patterns Protect Springtails 
PLoS ONE  2011;6(9):e25105.
Springtails, arthropods who live in soil, in decaying material, and on plants, have adapted to demanding conditions by evolving extremely effective and robust anti-adhesive skin patterns. However, details of these unique properties and their structural basis are still unknown. Here we demonstrate that collembolan skin can resist wetting by many organic liquids and at elevated pressures. We show that the combination of bristles and a comb-like hexagonal or rhombic mesh of interconnected nanoscopic granules distinguish the skin of springtails from anti-adhesive plant surfaces. Furthermore, the negative overhang in the profile of the ridges and granules were revealed to be a highly effective, but as yet neglected, design principle of collembolan skin. We suggest an explanation for the non-wetting characteristics of surfaces consisting of such profiles irrespective of the chemical composition. Many valuable opportunities arise from the translation of the described comb-like patterns and overhanging profiles of collembolan skin into man-made surfaces that combine stability against wear and friction with superior non-wetting and anti-adhesive characteristics.
PMCID: PMC3184130  PMID: 21980383

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