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1.  Dispersal and group formation dynamics in a rare and endangered temperate forest bat (Nyctalus lasiopterus, Chiroptera: Vespertilionidae) 
Ecology and Evolution  2016;6(22):8193-8204.
For elusive mammals like bats, colonization of new areas and colony formation are poorly understood, as is their relationship with the genetic structure of populations. Understanding dispersal and group formation behaviors is critical not only for a better comprehension of mammalian social dynamics, but also for guiding conservation efforts of rare and endangered species. Using nuclear and mitochondrial markers, we studied patterns of genetic diversity and differentiation among and within breeding colonies of giant noctule bats (Nyctalus lasiopterus), their relation to a new colony still in formation, and the impact of this ongoing process on the regionwide genetic makeup. Nuclear differentiation among colonies was relatively low and mostly nonsignificant. Mitochondrial variation followed this pattern, contrasting with findings for other temperate bat species. Our results suggest that this may indicate a recent population expansion. On average, female giant noctules were not more closely related to other colony members than to foreign individuals. This was also true for members of the newly forming colony and those of another, older group sampled shortly after its formation, suggesting that contrary to findings for other temperate bats, giant noctule colonies are not founded by relatives. However, mother–daughter pairs were found in the same populations more often than expected under random dispersal. Given this indication of philopatry, the lack of mitochondrial differentiation among most colonies in the region is probably due to the combination of a recent population expansion and group formation events.
PMCID: PMC5108270  PMID: 27878088
Colony formation; genetic structure; microsatellites; mtDNA; philopatry; relatedness
2.  Prevalence and clinical features of adverse food reactions in Portuguese adults 
Only one previous study, via telephone call, on the prevalence of self-reported food allergies has been performed in Portugal, in a small sample of adults. The objective of this study was to determine the prevalence of self-reported and probable food allergy, analyze the clinical features and involved foods in Portuguese adults.
Population-based, cross-sectional study performed in various healthcare centres from central Portugal. All 1436 randomly selected individuals (median age: 45 years, 50.6 % female) replied to a validated food allergy questionnaire by phone. Those who reported an adverse food reaction were invited to come to the hospital, where clinical history was taken, skin prick (SPT) and prick-prick skin (SPPT) tests were performed and food allergen-specific IgE levels (sIgE) were determined. An open oral challenge was performed in selected cases. Cases of positive clinical history of immediate (up to 2 h after ingestion) reaction in association with positive food sIgE levels and/or skin prick tests were classified as IgE-associated probable food allergy. Cases of positive clinical history of delayed (more than 2 h after ingestion) and negative food sIgE levels independently of positive SPT or SPPT results were classified as non-IgE associated probable food allergy.
The prevalence of probable food allergy in our sample was 1 %, with shellfish and fish as the most frequently implicated foods. IgE-mediated probable food allergy occurred in 0.71 % of cases, with shellfish, peanut and nuts mainly involved. Cutaneous symptoms were most frequently reported. Prevalence values and food types were discrepant between self-reported and probable food allergies.
The prevalence of probable food allergies in Portuguese adults is low, is mostly related to shellfish, peanut and nuts and most frequently involves cutaneous symptoms.
Electronic supplementary material
The online version of this article (doi:10.1186/s13223-016-0139-8) contains supplementary material, which is available to authorized users.
PMCID: PMC4975906  PMID: 27499765
Adverse food reaction; Food allergy; Adults; Prevalence; Cutaneous tests; Open food challenge
3.  Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress 
Age  2014;36(6):9721.
Maternal protein restriction (MPR) in pregnancy causes life course organ dysfunction, but few studies link the developmental origins of disease hypothesis to early aging. Suboptimal developmental nutrition increases oxidative stress (OS) and male infertility, damaging sperm function. We hypothesized that MPR in pregnancy accelerates age-related changes in testicular and sperm function related to both maternal diet and increased testicular OS in rat offspring. We studied male rats whose pregnant mothers ate either control (C, 20 % casein) or restricted (R, 10 % casein) isocaloric diet. After birth, mothers and offspring ate C diet. Testes were retrieved at 19 days gestation and across the life course (postnatal day (PND) 21, 36, 110, and 850) to measure OS markers, antioxidant enzymes, serum FSH, LH, and testosterone, and PND 110 sperm OS and quality. Fertility rate was evaluated at PND 110, 450, and 850. Offspring showed age- and MPR-related changes in testosterone, testicular OS markers and antioxidant enzymes and fertility, and maternal diet-related OS and sperm antioxidant enzyme changes. Developmental programming is considered a key factor in predisposing to chronic disease. Our data show that programming also plays an important role in aging trajectory. This interaction is a little studied area in aging biology that merits more investigation.
PMCID: PMC4213342  PMID: 25354645
Developmental programming; Testosterone; Sperm; Fertility; Aging; Maternal nutrition
4.  Seasonal Variation in Stable Carbon and Nitrogen Isotope Values of Bats Reflect Environmental Baselines 
PLoS ONE  2015;10(2):e0117052.
The stable carbon and nitrogen isotope composition of animal tissues is commonly used to trace wildlife diets and analyze food chains. Changes in an animal’s isotopic values over time are generally assumed to indicate diet shifts or, less frequently, physiological changes. Although plant isotopic values are known to correlate with climatic seasonality, only a few studies restricted to aquatic environments have investigated whether temporal isotopic varia-tion in consumers may also reflect environmental baselines through trophic propagation. We modeled the monthly variation in carbon and nitrogen isotope values in whole blood of four insectivorous bat species occupying different foraging niches in southern Spain. We found a common pattern of isotopic variation independent of feeding habits, with an overall change as large as or larger than one trophic step. Physiological changes related to reproduction or to fat deposition prior to hibernation had no effect on isotopic variation, but juvenile bats had higher δ13C and δ15N values than adults. Aridity was the factor that best explained isotopic variation: bat blood became enriched in both 13C and 15N after hotter and/or drier periods. Our study is the first to show that consumers in terrestrial ecosystems reflect seasonal environmental dynamics in their isotope values. We highlight the danger of misinterpreting stable isotope data when not accounting for seasonal isotopic baselines in food web studies. Understanding how environmental seasonality is inte-grated in animals’ isotope values will be crucial for developing reliable methods to use stable isotopes as dietary tracers.
PMCID: PMC4336313  PMID: 25700080
5.  Topographical transcriptome mapping of the mouse medial ganglionic eminence by spatially resolved RNA-seq 
Genome Biology  2014;15(10):486.
Cortical interneurons originating from the medial ganglionic eminence, MGE, are among the most diverse cells within the CNS. Different pools of proliferating progenitor cells are thought to exist in the ventricular zone of the MGE, but whether the underlying subventricular and mantle regions of the MGE are spatially patterned has not yet been addressed. Here, we combined laser-capture microdissection and multiplex RNA-sequencing to map the transcriptome of MGE cells at a spatial resolution of 50 μm.
Distinct groups of progenitor cells showing different stages of interneuron maturation are identified and topographically mapped based on their genome-wide transcriptional pattern. Although proliferating potential decreased rather abruptly outside the ventricular zone, a ventro-lateral gradient of increasing migratory capacity was identified, revealing heterogeneous cell populations within this neurogenic structure.
We demonstrate that spatially resolved RNA-seq is ideally suited for high resolution topographical mapping of genome-wide gene expression in heterogeneous anatomical structures such as the mammalian central nervous system.
Electronic supplementary material
The online version of this article (doi:10.1186/s13059-014-0486-z) contains supplementary material, which is available to authorized users.
PMCID: PMC4234883  PMID: 25344199
6.  Crowding in the City: Losing and Winning Competitors of an Invasive Bird 
PLoS ONE  2014;9(6):e100593.
Invasive species can take advantage of resources unexploited by natives (opportunism hypothesis) or they can exploit the same resources but more aggressively or efficiently (competition hypothesis), thus impacting native species. However, invasive species tend to exploit anthropogenic habitats that are inefficiently used by natives such as urban environments. Focusing on the ring-necked parakeet (Psittacula krameri), one of the most invasive birds worldwide, we combined observations of interspecific aggressions, species-specific cavity-nest preferences and the spatial distribution of the native cavity-nesting vertebrate community to determine the invasion process as well as its potential impacts on native species in a Mediterranean city. Our results support the competition hypothesis, suggesting that ring-necked parakeets are outcompeting native species sharing nest-site preferences. Parakeets initiated and won most interspecific aggressions, which were directed towards competitors but also towards predators. This behaviour could explain the spatial arrangement of natives, with most bird species breeding close to parakeets possibly to take advantage of their effective antipredatory behaviour. However, temporal and spatial patterns of segregation suggest that a threatened bat species is negatively affected by parakeets. This demonstrates that common species gain benefits and threatened ones (in this study, a bat and possibly a falcon) lose nest sites due to invaders. Therefore, the conservation status of the native species that pay the costs of competition with invaders should be considered. This scenario of winners and losers may, however, shift towards more losers if the ring-necked parakeet population continues to grow, thus requiring close monitoring and control/eradication programs to avoid further impacts.
PMCID: PMC4063952  PMID: 24945439
7.  Novel Papillomaviruses in Free-Ranging Iberian Bats: No Virus–Host Co-evolution, No Strict Host Specificity, and Hints for Recombination 
Genome Biology and Evolution  2014;6(1):94-104.
Papillomaviruses (PVs) are widespread pathogens. However, the extent of PV infections in bats remains largely unknown. This work represents the first comprehensive study of PVs in Iberian bats. We identified four novel PVs in the mucosa of free-ranging Eptesicus serotinus (EserPV1, EserPV2, and EserPV3) and Rhinolophus ferrumequinum (RferPV1) individuals and analyzed their phylogenetic relationships within the viral family. We further assessed their prevalence in different populations of E. serotinus and its close relative E. isabellinus. Although it is frequent to read that PVs co-evolve with their host, that PVs are highly species-specific, and that PVs do not usually recombine, our results suggest otherwise. First, strict virus–host co-evolution is rejected by the existence of five, distantly related bat PV lineages and by the lack of congruence between bats and bat PVs phylogenies. Second, the ability of EserPV2 and EserPV3 to infect two different bat species (E. serotinus and E. isabellinus) argues against strict host specificity. Finally, the description of a second noncoding region in the RferPV1 genome reinforces the view of an increased susceptibility to recombination in the E2-L2 genomic region. These findings prompt the question of whether the prevailing paradigms regarding PVs evolution should be reconsidered.
PMCID: PMC3914694  PMID: 24391150
bats; papillomavirus; evolution; phylogeny; biodiversity; wildlife
8.  Critical Role of GFRα1 in the Development and Function of the Main Olfactory System 
Glial cell line-derived neurotrophic factor (GDNF) and its receptor GFRα1 are prominently expressed in the olfactory epithelium (OE) and olfactory bulb (OB), but their importance for olfactory system development is completely unknown. We have investigated the consequences of GFRα1 deficiency for mouse olfactory system development and function. In the OE, GFRα1 was expressed in basal precursors, immature olfactory sensory neurons (OSNs), and olfactory ensheathing cells (OECs), but was excluded from mature OSNs. The OE of newborn Gfra1 knock-out mice was thinner and contained fewer OSNs, but more dividing precursors, suggesting deficient neurogenesis. Immature OSN axon bundles were enlarged and associated OECs increased, indicating impaired migration of OECs and OSN axons. In the OB, GFRα1 was expressed in immature OSN axons and OECs of the nerve layer, as well as mitral and tufted cells, but was excluded from GABAergic interneurons. In newborn knock-outs, the nerve layer was dramatically reduced, exhibiting fewer axons and OECs. Bulbs were smaller and presented fewer and disorganized glomeruli and a significant reduction in mitral cells. Numbers of tyrosine hydroxylase-, calbindin-, and calretinin-expressing interneurons were also reduced in newborn mice lacking GFRa1. At birth, the OE and OB of Gdnf knock-out mice displayed comparable phenotypes. Similar deficits were also found in adult heterozygous Gfra1+/− mutants, which in addition displayed diminished responses in behavioral tests of olfactory function. We conclude that GFRα1 is critical for the development and function of the main olfactory system, contributing to the development and allocation of all major classes of neurons and glial cells.
PMCID: PMC3655334  PMID: 23197722
9.  A Triple-Isotope Approach to Predict the Breeding Origins of European Bats 
PLoS ONE  2012;7(1):e30388.
Despite a commitment by the European Union to protect its migratory bat populations, conservation efforts are hindered by a poor understanding of bat migratory strategies and connectivity between breeding and wintering grounds. Traditional methods like mark-recapture are ineffective to study broad-scale bat migratory patterns. Stable hydrogen isotopes (δD) have been proven useful in establishing spatial migratory connectivity of animal populations. Before applying this tool, the method was calibrated using bat samples of known origin. Here we established the potential of δD as a robust geographical tracer of breeding origins of European bats by measuring δD in hair of five sedentary bat species from 45 locations throughout Europe. The δD of bat hair strongly correlated with well-established spatial isotopic patterns in mean annual precipitation in Europe, and therefore was highly correlated with latitude. We calculated a linear mixed-effects model, with species as random effect, linking δD of bat hair to precipitation δD of the areas of hair growth. This model can be used to predict breeding origins of European migrating bats. We used δ13C and δ15N to discriminate among potential origins of bats, and found that these isotopes can be used as variables to further refine origin predictions. A triple-isotope approach could thereby pinpoint populations or subpopulations that have distinct origins. Our results further corroborated stable isotope analysis as a powerful method to delineate animal migrations in Europe.
PMCID: PMC3264582  PMID: 22291947
10.  Detection of alpha and betacoronaviruses in multiple Iberian bat species 
Archives of Virology  2011;156(10):1883-1890.
Bat coronaviruses (CoV) are putative precursors of the severe acute respiratory syndrome (SARS) CoV and other CoV that crossed the species barrier from zoonotic reservoirs into the human population. To determine the presence and distribution of CoV in Iberian bats, 576 individuals of 26 different bat species were captured in 13 locations in Spain. We report for the first time the presence of 14 coronaviruses in 9 Iberian bat species. Phylogenetic analysis of a conserved CoV genome region (RdRp gene) shows a wide diversity and distribution of alpha and betacoronavirus in Spain. Interestingly, although some of these viruses are related to other European BatCoV, or to Asian CoV, some of the viruses found in Spain cluster in new groups of α and β CoV.
PMCID: PMC3181409  PMID: 21766197
11.  Phylogeny of European Bat Lyssavirus 1 in Eptesicus isabellinus Bats, Spain 
Emerging Infectious Diseases  2011;17(3):520-523.
To better understand the epidemiology of European bat lyssavirus 1 (EBLV-1) in Europe, we phylogenetically characterized Lyssavirus from Eptesicus isabellinus bats in Spain. An independent cluster of EBLV-1 possibly resulted from geographic isolation and association with a different reservoir from other European strains. EBLV-1 phylogeny is complex and probably associated with host evolutionary history.
PMCID: PMC3166003  PMID: 21392449
Lyssavirus; bats; phylogeny; rabies; EBLV-1; Eptesicus isabellinus; viruses; Spain; dispatch
12.  Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers 
Neuron  2009;62(1):72-83.
Ligand-mediated dimerization has emerged as a universal mechanism of growth factor receptor activation. Recent structural studies have shown that neurotrophins interact with dimers of the p75 neurotrophin receptor (p75NTR), but the actual mechanism of receptor activation has remained elusive. Here we show that p75NTR forms disulphide-linked dimers independently of neurotrophin binding through the highly conserved Cys257 in its transmembrane domain. Mutation of Cys257 abolished neurotrophin-dependent receptor activity but did not affect downstream signaling by the p75NTR/NgR/Lingo-1 complex in response to MAG, indicating the existence of distinct, ligand-specific activation mechanisms for p75NTR. FRET experiments revealed a close association of p75NTR intracellular domains that was transiently disrupted by conformational changes induced upon NGF binding. Although mutation of Cys257 did not alter the oligomeric state of p75NTR, the mutant receptor was no longer able to propagate conformational changes to the cytoplasmic domain upon ligand binding. We propose that neurotrophins activate p75NTR by a novel mechanism involving rearrangement of disulphide-linked receptor subunits.
PMCID: PMC2810632  PMID: 19376068
13.  Endemic Circulation of European Bat Lyssavirus Type 1 in Serotine Bats, Spain 
Emerging Infectious Diseases  2008;14(8):1263-1266.
To determine the presence of European bat lyssavirus type 1 in southern Spain, we studied 19 colonies of serotine bats (Eptesicus isabellinus), its main reservoir, during 1998–2003. Viral genome and antibodies were detected in healthy bats, which suggests subclinical infection. The different temporal patterns of circulation found in each colony indicate independent endemic circulation.
PMCID: PMC2600403  PMID: 18680651
lyssavirus; bats; surveillance; rabies; dispatch
14.  Bats' Conquest of a Formidable Foraging Niche: The Myriads of Nocturnally Migrating Songbirds 
PLoS ONE  2007;2(2):e205.
Along food chains, i.e., at different trophic levels, the most abundant taxa often represent exceptional food reservoirs, and are hence the main target of consumers and predators. The capacity of an individual consumer to opportunistically switch towards an abundant food source, for instance, a prey that suddenly becomes available in its environment, may offer such strong selective advantages that ecological innovations may appear and spread rapidly. New predator-prey relationships are likely to evolve even faster when a diet switch involves the exploitation of an unsaturated resource for which few or no other species compete. Using stable isotopes of carbon and nitrogen as dietary tracers, we provide here strong support to the controversial hypothesis that the giant noctule bat Nyctalus lasiopterus feeds on the wing upon the multitude of flying passerines during their nocturnal migratory journeys, a resource which, while showing a predictable distribution in space and time, is only seasonally available. So far, no predator had been reported to exploit this extraordinarily diverse and abundant food reservoir represented by nocturnally migrating passerines.
PMCID: PMC1784064  PMID: 17299585
15.  ALK7, a Receptor for Nodal, Is Dispensable for Embryogenesis and Left-Right Patterning in the Mouse 
Molecular and Cellular Biology  2004;24(21):9383-9389.
Mesendoderm formation and left-right patterning during vertebrate development depend upon selected members of the transforming growth factor β superfamily, particularly Nodal and Nodal-related ligands. Two type I serine/threonine kinase receptors have been identified for Nodal, ALK4 and ALK7. Mouse embryos lacking ALK4 fail to produce mesendoderm and die shortly after gastrulation, resembling the phenotype of Nodal knockout mice. Whether ALK4 contributes to left-right patterning is still unknown. Here we report the generation and initial characterization of mice lacking ALK7. Homozygous mutant mice were born at the expected frequency and remained viable and fertile. Viability at weaning was not different from that of the wild type in ALK7−/−; Nodal+/− and ALK7−/−; ALK4+/− compound mutants. ALK7 and ALK4 were highly expressed in interdigital regions of the developing limb bud. However, ALK7 mutant mice displayed no skeletal abnormalities or limb malformations. None of the left-right patterning abnormalities and organogenesis defects identified in mice carrying mutations in Nodal or in genes encoding ActRIIA and ActRIIB coreceptors, including heart malformations, pulmonary isomerism, right-sided gut, and spleen hypoplasia, were observed in mice lacking ALK7. Finally, the histological organization of the cerebellum, cortex, and hippocampus, all sites of significant ALK7 expression in the rodent brain, appeared normal in ALK7 mutant mice. We conclude that ALK7 is not an essential mediator of Nodal signaling during mesendoderm formation and left-right patterning in the mouse but may instead mediate other activities of Nodal and related ligands in the development or function of particular tissues and organs.
PMCID: PMC522223  PMID: 15485907
16.  Cross-talk between the Notch and TGF-β signaling pathways mediated by interaction of the Notch intracellular domain with Smad3 
The Journal of Cell Biology  2003;163(4):723-728.
The Notch and transforming growth factor-β (TGF-β) signaling pathways play critical roles in the control of cell fate during metazoan development. However, mechanisms of cross-talk and signal integration between the two systems are unknown. Here, we demonstrate a functional synergism between Notch and TGF-β signaling in the regulation of Hes-1, a direct target of the Notch pathway. Activation of TGF-β signaling up-regulated Hes-1 expression in vitro and in vivo. This effect was abrogated in myogenic cells by a dominant-negative form of CSL, an essential DNA-binding component of the Notch pathway. TGF-β regulated transcription from the Hes-1 promoter in a Notch-dependent manner, and the intracellular domain of Notch1 (NICD) cooperated synergistically with Smad3, an intracellular transducer of TGF-β signals, to induce the activation of synthetic promoters containing multimerized CSL- or Smad3-binding sites. NICD and Smad3 were shown to interact directly, both in vitro and in cells, in a ligand-dependent manner, and Smad3 could be recruited to CSL-binding sites on DNA in the presence of CSL and NICD. These findings indicate that Notch and TGF-β signals are integrated by direct protein–protein interactions between the signal-transducing intracellular elements from both pathways.
PMCID: PMC2173673  PMID: 14638857
Hes-1; C2C12; CSL; Smad4; neural stem cell
17.  Screening of Active Lyssavirus Infection in Wild Bat Populations by Viral RNA Detection on Oropharyngeal Swabs 
Journal of Clinical Microbiology  2001;39(10):3678-3683.
Brain analysis cannot be used for the investigation of active lyssavirus infection in healthy bats because most bat species are protected by conservation directives. Consequently, serology remains the only tool for performing virological studies on natural bat populations; however, the presence of antibodies merely reflects past exposure to the virus and is not a valid marker of active infection. This work describes a new nested reverse transcription (RT)-PCR technique specifically designed for the detection of the European bat virus 1 on oropharyngeal swabs obtained from bats but also able to amplify RNA from the remaining rabies-related lyssaviruses in brain samples. The technique was successfully used for surveillance of a serotine bat (Eptesicus serotinus) colony involved in a case of human exposure, in which 15 out of 71 oropharyngeal swabs were positive. Lyssavirus infection was detected on 13 oropharyngeal swabs but in only 5 brains out of the 34 animals from which simultaneous brain and oropharyngeal samples had been taken. The lyssavirus involved could be rapidly identified by automatic sequencing of the RT-PCR products obtained from 14 brains and three bat oropharyngeal swabs. In conclusion, RT-PCR using oropharyngeal swabs will permit screening of wild bat populations for active lyssavirus infection, for research or epidemiological purposes, in line not only with conservation policies but also in a more efficient manner than classical detection techniques used on the brain.
PMCID: PMC88406  PMID: 11574590
18.  The shaping of genetic variation in edge-of-range populations under past and future climate change 
Ecology Letters  2013;16(10):1258-1266.
With rates of climate change exceeding the rate at which many species are able to shift their range or adapt, it is important to understand how future changes are likely to affect biodiversity at all levels of organisation. Understanding past responses and extent of niche conservatism in climatic tolerance can help predict future consequences. We use an integrated approach to determine the genetic consequences of past and future climate changes on a bat species, Plecotus austriacus. Glacial refugia predicted by palaeo-modelling match those identified from analyses of extant genetic diversity and model-based inference of demographic history. Former refugial populations currently contain disproportionately high genetic diversity, but niche conservatism, shifts in suitable areas and barriers to migration mean that these hotspots of genetic diversity are under threat from future climate change. Evidence of population decline despite recent northward migration highlights the need to conserve leading-edge populations for spearheading future range shifts.
PMCID: PMC4015367  PMID: 23890483
Approximate Bayesian computation; Chiroptera; ecological niche modelling; niche conservatism; phylogeography

Results 1-18 (18)