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1.  Species-specific differences in relative eye size are related to patterns of edge avoidance in an Amazonian rainforest bird community 
Ecology and Evolution  2014;4(19):3736-3745.
Eye size shows a large degree of variation among species, even after correcting for body size. In birds, relatively larger eyes have been linked to predation risk, capture of mobile prey, and nocturnal habits. Relatively larger eyes enhance visual acuity and also allow birds to forage and communicate in low-light situations. Complex habitats such as tropical rain forests provide a mosaic of diverse lighting conditions, including differences among forest strata and at different distances from the forest edge. We examined in an Amazonian forest bird community whether microhabitat occupancy (defined by edge avoidance and forest stratum) was a predictor of relative eye size. We found that relative eye size increased with edge avoidance, but did not differ according to forest stratum. Nevertheless, the relationship between edge avoidance and relative eye size showed a nonsignificant positive trend for species that inhabit lower forest strata. Our analysis shows that birds that avoid forest edges have larger eyes than those living in lighter parts. We expect that this adaptation may allow birds to increase their active daily period in dim areas of the forest. The pattern that we found raises the question of what factors may limit the evolution of large eyes.
PMCID: PMC4301040  PMID: 25614788
Avian vision; ecology; habitat use; light environment; perception
2.  The PHA Test as an Indicator of Phagocytic Activity in a Passerine Bird 
PLoS ONE  2013;8(12):e84108.
Several techniques in ecological immunology have been used to assess bird immunocompetence thus providing useful information to understand the contribution of the immunological system in life-history decisions. The phytohaemagglutinin (PHA)-skin test has been the most widely employed technique being interpreted as the sole result of T lymphocytes proliferation and hence used to evaluate acquired immunological capacity. However, the presence of high numbers of phagocytic cells in the swelling point has cast some doubt about such an assumption. To address this issue, we collected blood from 14 days-old nestlings of spotless starling (Sturnus unicolor), administered subcutaneous PHA immediately after and then measured the swelling response 24 hours later. Differential counts of white blood cells suggested that an intense development of acquired immunological defences was taking place. The phagocytic activity of both heterophiles and monocytes was also very intense as it was the swelling response. Moreover, our results show, for the first time in birds, a positive relationship between the phagocytic activity of both kinds of cells and the swelling response. This broadens the significance of the PHA test from reflecting T lymphocytes proliferation -as previously proposed but still undetermined in vivo- to evaluate phagocytosis as well. In other words, our data suggest that the PHA swelling response may not be considered as the only consequence of processes of specific and induced immunity –T lymphocytes proliferation- but also of constitutive and nonspecific immunity –heterophiles and monocytes phagocytosis. We propose the extensive use of PHA-skin test as an optimal technique to assess immunocompetence.
PMCID: PMC3877195  PMID: 24391896
4.  Dishevelled Proteins Are Associated with Olfactory Sensory Neuron Presynaptic Terminals 
PLoS ONE  2013;8(2):e56561.
Olfactory sensory neurons (OSNs) project their axons from the olfactory epithelium toward the olfactory bulb (OB) in a heterogeneous and unsorted arrangement. However, as the axons approach the glomerular layer of the OB, axons from OSNs expressing the same odorant receptor (OR) sort and converge to form molecularly homogeneous glomeruli. Axon guidance cues, cell adhesion molecules, and OR induced activity have been implicated in the final targeting of OSN axons to specific glomeruli. Less understood, and often controversial, are the mechanisms used by OSN axons to initially navigate from the OE toward the OB. We previously demonstrated a role for Wnt and Frizzled (Fz) molecules in OSN axon extension and organization within the olfactory nerve. Building on that we now turned our attention to the downstream signaling cascades from Wnt-Fz interactions. Dishevelled (Dvl) is a key molecule downstream of Fz receptors. Three isoforms of Dvl with specific as well as overlapping functions are found in mammals. Here, we show that Dvl-1 expression is restricted to OSNs in the dorsal recess of the nasal cavity, and labels a unique subpopulation of glomeruli. Dvl-2 and Dvl-3 have a widespread distribution in both the OE and OB. Both Dvl-1 and Dvl-2 are associated with intra-glomerular pre-synaptic OSN terminals, suggesting a role in synapse formation/stabilization. Moreover, because Dvl proteins were observed in all OSN axons, we hypothesize that they are important determinants of OSN cell differentiation and axon extension.
PMCID: PMC3577874  PMID: 23437169
5.  Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird 
Biology Letters  2010;7(1):36-38.
Research has shown that bird songs are modified in different ways to deal with urban noise and promote signal transmission through noisy environments. Urban noise is composed of low frequencies, thus the observation that songs have a higher minimum frequency in noisy places suggests this is a way of avoiding noise masking. Most studies are correlative and there is as yet little experimental evidence that this is a short-term mechanism owing to individual plasticity. Here we experimentally test if house finches (Carpodacus mexicanus) can modulate the minimum frequency of their songs in response to different noise levels. We exposed singing males to three continuous treatments: low–high–low noise levels. We found a significant increase in minimum frequency from low to high and a decrement from high to low treatments. We also found that this was mostly achieved by modifying the frequency of the same low-frequency syllable types used in the different treatments. When different low-frequency syllables were used, those sung during the noisy condition were longer than the ones sang during the quiet condition. We conclude that house finches modify their songs in several ways in response to urban noise, thus providing evidence of a short-term acoustic adaptation.
PMCID: PMC3030866  PMID: 20610421
house finch; Carpodacus mexicanus; birdsong; urban noise; acoustic adaptation
6.  Renal Cystic Disease Proteins Play Critical Roles in the Organization of the Olfactory Epithelium 
PLoS ONE  2011;6(5):e19694.
It was reported that some proteins known to cause renal cystic disease (NPHP6; BBS1, and BBS4) also localize to the olfactory epithelium (OE), and that mutations in these proteins can cause anosmia in addition to renal cystic disease. We demonstrate here that a number of other proteins associated with renal cystic diseases – polycystin 1 and 2 (PC1, PC2), and Meckel-Gruber syndrome 1 and 3 (MKS1, MKS3) – localize to the murine OE. PC1, PC2, MKS1 and MKS3 are all detected in the OE by RT-PCR. We find that MKS3 localizes specifically to dendritic knobs of olfactory sensory neurons (OSNs), while PC1 localizes to both dendritic knobs and cilia of mature OSNs. In mice carrying mutations in MKS1, the expression of the olfactory adenylate cyclase (AC3) is substantially reduced. Moreover, in rats with renal cystic disease caused by a mutation in MKS3, the laminar organization of the OE is perturbed and there is a reduced expression of components of the odor transduction cascade (Golf, AC3) and α-acetylated tubulin. Furthermore, we show with electron microscopy that cilia in MKS3 mutant animals do not manifest the proper microtubule architecture. Both MKS1 and MKS3 mutant animals show no obvious alterations in odor receptor expression. These data show that multiple renal cystic proteins localize to the OE, where we speculate that they work together to regulate aspects of the development, maintenance or physiological activities of cilia.
PMCID: PMC3094399  PMID: 21614130
7.  Chromosomal location-dependent non-stochastic onset of odor receptor expression 
As odorant receptors (ORs) are thought to be critical determinants of olfactory sensory neuron (OSN) axon targeting and organization, we examined the spatiotemporal onset of mice ORs expression from the differentiation of OSNs in the olfactory placode to an aging olfactory epithelium. ORs were first detected in the placode at embryonic (E) day 9, at the onset of OSN differentiation but prior to axon extension. By E13, 22/23 ORs were expressed. Onset of individual OR expression was diverse; levels and patterns of expression were unique for each OR. Regional distribution of ORs within OE zones appeared stable across development; adult-like patterns were observed by E13. Finally, analysis of OR expression and chromosomal location suggests that ORs are not stochastically expressed; they show evidence of coordinated expression. Collectively, these studies demonstrate that ORs are not equally represented in the “olfactome” across an animal’s lifespan.
PMCID: PMC2921185  PMID: 20668191
8.  Blood Vessels Form a Migratory Scaffold in the Rostral Migratory Stream 
In adult mice, new neurons born in the subventricular zone (SVZ), lining the lateral ventricles, migrate tangentially into the olfactory bulb along a well-delineated path, the Rostral Migratory Stream (RMS). Neuroblasts in the RMS migrate tangentially in chains, without a recognized migratory scaffold. Here, we quantitatively examine the distribution of, and relationships between, cells within the RMS, throughout its rostral-caudal extent. We show that there is a higher density of blood vessels in the RMS than in other brain regions, including areas with equal cell density, and that the orientation of blood vessels parallels the RMS throughout the caudal to rostral path. Of particular interest, migratory neuroblast chains are longitudinally aligned along blood vessels within the RMS, with over 80% of vessel length in rostral areas of the RMS apposed by neuroblasts. Electron micrographs show direct contact between endothelial cells and neuroblasts, although intervening astrocytic processes are often present. Within the RMS, astrocytes arborize extensively, extending long processes which are parallel to blood vessels and the direction of neuroblast migration. Thus, the astrocytic processes establish a longitudinal alignment within the RMS, rather than a more typical stellate shape. This complementary alignment suggests that blood vessels and astrocytes may cooperatively establish a scaffold for migrating neuroblasts, as well as provide and regulate migratory cues.
PMCID: PMC2746017  PMID: 19575445
Neuroblast migration; olfactory bulb; subventricular zone; glia; mouse; adult neurogenesis; astrocyte; endothelium
Odorant receptors are thought to be critical determinants of olfactory sensory neuron axon targeting and organization. Nonetheless, a systematic characterization of the onset of odorant receptor expression has not yet been done in the main olfactory epithelium. Here, we briefly review our current understanding regarding the onset of odorant receptor expression in the main olfactory epithelium and identify some of those questions which we believe must be of high priority for future study.
PMCID: PMC2729770  PMID: 19686100
olfactory epithelium; development; axon guidance
10.  Wnt/Frizzled Family Members Mediate Olfactory Sensory Neuron Axon Extension 
A comprehensive model has yet to emerge, but it seems likely that numerous mechanisms contribute to the specificity of olfactory sensory neuron (OSN) axon innervation of the olfactory bulb. Elsewhere in the nervous system the Wnt/Fz family has been implicated in patterning of anterior-posterior axes, cell type specification, cell proliferation and axon guidance. Because of our work describing cadherin-catenin family member expression in the primary olfactory pathway, and because mechanisms of Wnt-Fz interactions can depend in part on catenins, we were encouraged to explore Wnt-Fz expression and function in OSN axon extension. Here, we show that OSNs express Fz-1, -3, and Wnt-5a, while olfactory ensheathing cells (OECs) express Wnt-4. Fz-7 is also expressed in the olfactory nerve by cells that delineate large axon fascicles, but are negative for OEC markers. Fz-1 showed a developmental down-regulation. However, in adults it is expressed at different levels across the olfactory epithelium and in restricted glomeruli across the olfactory bulb, suggesting an important role in the formation and maintenance of OSN connections to the olfactory bulb. Reporter TOPGAL mice demonstrated that some OECs located in the inner olfactory nerve layer can respond to Wnt ligands. Of further interest, we show here with in vitro assays that Wnt-5a increases OSN axon outgrowth and alters growth cone morphology. Our data point to a key role for Wnt/Fz molecules in the development of the mouse olfactory system, providing complementary mechanisms required for OSN axon extension and coalescence.
PMCID: PMC2570497  PMID: 18803244
Olfactory Epithelium; Olfactory Bulb; Glomeruli; Olfactory Ensheathing Cell; Olfactory Pathway; Growth Cones
11.  Adaptive developmental plasticity in growing nestlings: sibling competition induces differential gape growth 
Sibling competition has been shown to affect overall growth rates in birds. However, growth consists on the coordinated development of a multitude of structures, and there is ample scope for developmental plasticity and trade-offs among these structures. We would expect that the growth of structures that are used in sibling competition, such as the gape of altricial nestlings, should be prioritized under intense competition. We conducted an experiment in the spotless starling (Sturnus unicolor), cross-fostering nestlings to nests with different levels of sibling competition. We predicted that nestlings subjected to higher levels of sibling competition should develop larger gapes than control birds. We found that, halfway through the nestling period, overall size (a composite index of mass, wing, tarsus and bill) was reduced in nests with intense sibling competition, whereas gape width remained unaffected. At the end of the nestling period, experimental nestlings had wider gapes than controls. Additionally, a correlative study showed that nestling gape width increased when feeding conditions worsened and overall size decreased. These patterns could either be due to increased growth of gape flanges or to delayed reabsorption of this structure. Our results show that birds can invest differentially in the development of organs during growth, and that the growth of organs used in sibling competition is prioritized over structural growth.
PMCID: PMC2596805  PMID: 18089540
differential growth; sibling competition; spotless starling; nutritional stress; developmental plasticity; gape width
12.  Principles of Glomerular Organization in the Human Olfactory Bulb – Implications for Odor Processing 
PLoS ONE  2008;3(7):e2640.
Olfactory sensory neurons (OSN) in mice express only 1 of a possible 1,100 odor receptors (OR) and axons from OSNs expressing the same odor receptor converge into ∼2 of the 1,800 glomeruli in each olfactory bulb (OB) in mice; this yields a convergence ratio that approximates 2∶1, 2 glomeruli/OR. Because humans express only 350 intact ORs, we examined human OBs to determine if the glomerular convergence ratio of 2∶1 established in mice was applicable to humans. Unexpectedly, the average number of human OB glomeruli is >5,500 yielding a convergence ratio of ∼16∶1. The data suggest that the initial coding of odor information in the human OB may differ from the models developed for rodents and that recruitment of additional glomeruli for subpopulations of ORs may contribute to more robust odor representation.
PMCID: PMC2440537  PMID: 18612420
13.  Maternal developmental stress reduces reproductive success of female offspring in zebra finches 
Environmental factors play a key role in the expression of phenotypic traits and life-history decisions, specifically when they act during early development. In birds, brood size is a main environmental factor affecting development. Experimental manipulation of brood sizes can result in reduced offspring condition, indicating that developmental deficits in enlarged broods have consequences within the affected generation. Yet, it is unclear whether stress during early development can have fitness consequences projecting into the next generation. To study such trans-generational fitness effects, we bred female zebra finches, Taeniopygia guttata, whose mothers had been raised in different experimental brood sizes. We found that adult females were increasingly smaller with increasing experimental brood size in which their mother had been raised. Furthermore, reproductive success at hatching and fledging covaried negatively with the experimental brood size in which their mothers were raised. These results illustrate that early developmental stress can have long-lasting effects affecting reproductive success of future generations. Such trans-generational effects can be life-history responses adapted to environmental conditions experienced early in life.
PMCID: PMC1634771  PMID: 16822750
early developmental stress; maternal effects; thrifty phenotype; trans-generational fitness effects; zebra finch
14.  Nestling immunocompetence and testosterone covary with brood size in a songbird. 
The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross-fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell-mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.
PMCID: PMC1691669  PMID: 15255102
15.  Transgenerational effects on body size caused by early developmental stress in zebra finches 
Biology Letters  2005;1(1):95-97.
The nutritional and social conditions that individuals experience during early development can have profound effects on their morphology, physiology, behaviour and life history. Experimental increases in brood size in birds can result in reduced offspring condition and survival, indicating that developmental deficits in enlarged broods have negative fitness consequences within the affected generation. To study long-term effects (i.e. transgenerational effects of developmental stress), we conducted a two-step breeding experiment in which we manipulated early developmental conditions in zebra finches Taeniopygia guttata. We raised zebra finches by manipulating brood sizes and controlled for maternal and genetic effects by cross-fostering. In a previous study, we showed that offspring condition and body size decreased with increasing brood size. Here we show that this effect was carried over to the next generation. Body size in nestlings and at nutritional independence was affected by the brood size in which the mothers were raised. Female offspring did significantly worse than male offspring when the mother had been raised in large broods, suggesting a sex-specific influence of maternal effects. These findings link early developmental stress in females with the phenotype of the next generation via maternal effects.
PMCID: PMC1629067  PMID: 17148137
cross-fostering; early developmental stress; life history; maternal effects; zebra finch
16.  Non-exclusive exclusion (Commentary on Capello et al.) 
PMCID: PMC2695854  PMID: 19200069

Results 1-16 (16)