Investigating the Relationship between Topology and Evolution in a Dynamic Nematode Odor Genetic Network

The relationship between biological network architectures and evolution is unclear. Within the phylum nematoda olfaction represents a critical survival tool. For nematodes, olfaction contributes to multiple processes including the finding of food, hosts, and reproductive partners, making developmental decisions, and evading predators. Here we examine a dynamic nematode odor genetic network to investigate how divergence, diversity, and contribution are shaped by network topology. Our findings describe connectivity frameworks and characteristics that correlate with molecular evolution and contribution across the olfactory network. Our data helps guide the development of a robust evolutionary description of the nematode odor network that may eventually aid in the prediction of interactive and functional qualities of novel nodes

A comparative study of the molecular evolution of signalling pathway members across olfactory, gustatory and photosensory modalities

All sensory modalities serve a similar objective, which is to decode input by making predictions in time and space about an animal’s surroundings. The evolution of sensory modalities is driven by the need to shape effective behavioural outputs, and in turn increase survival. Throughout evolution, sensory systems have undergone a great deal of specialization; and even though some modalities are derived from unique origins within different phyla, they still exhibit many common design features (Strausfeld and Hildebrand 1999; Eisthen 2002; Jacobs et al. 2007). We now have detailed mechanistic data on how sensory systems operate within specific animals (Buck and Axel 1991; Chalasani et al. 2007; Sato et al. 2008; Wicher et al. 2008), however it is still not clear how sensory signalling pathways evolve at the molecular level, and whether these evolutionary mechanisms are shared between diverse taxa. Here we set out to investigate the molecular evolution of signalling pathway members across olfactory, gustatory, and photosensory modalities from very divergent phyla in an attempt to develop a model of molecular evolution for sensory systems. From our pairwise intraphylum analysis we found that sensory signalling pathways unusually undergo high levels of functional constraint that are higher than genomewide global levels of constraint, and this purifying selection is common within the very divergent taxa we examined. We also find that gene duplication events represent a conserved but heterogeneous driver of evolution within sensory signalling pathways. Taken together, we propose a ‘sessile’ mechanism of sensory signalling pathway evolution, which on one side facilitates bursts of gene duplication and relaxed selection and on the other side it is unusually anchored by high levels of selective constraint that preserves core sensory function

A comparative study of the molecular evolution of signalling pathway members across olfactory, gustatory and photosensory modalities

All sensory modalities serve a similar objective, which is to decode input by making predictions in time and space about an animal’s surroundings. The evolution of sensory modalities is driven by the need to shape effective behavioural outputs, and in turn increase survival. Throughout evolution, sensory systems have undergone a great deal of specialization; and even though some modalities are derived from unique origins within different phyla, they still exhibit many common design features (Strausfeld and Hildebrand 1999; Eisthen 2002; Jacobs et al. 2007). We now have detailed mechanistic data on how sensory systems operate within specific animals (Buck and Axel 1991; Chalasani et al. 2007; Sato et al. 2008; Wicher et al. 2008), however it is still not clear how sensory signalling pathways evolve at the molecular level, and whether these evolutionary mechanisms are shared between diverse taxa. Here we set out to investigate the molecular evolution of signalling pathway members across olfactory, gustatory, and photosensory modalities from very divergent phyla in an attempt to develop a model of molecular evolution for sensory systems. From our pairwise intraphylum analysis we found that sensory signalling pathways unusually undergo high levels of functional constraint that are higher than genomewide global levels of constraint, and this purifying selection is common within the very divergent taxa we examined. We also find that gene duplication events represent a conserved but heterogeneous driver of evolution within sensory signalling pathways. Taken together, we propose a ‘sessile’ mechanism of sensory signalling pathway evolution, which on one side facilitates bursts of gene duplication and relaxed selection and on the other side it is unusually anchored by high levels of selective constraint that preserves core sensory function

Multiple lineage specific expansions within the guanylyl cyclase gene family

BACKGROUND: Guanylyl cyclases (GCs) are responsible for the production of the secondary messenger cyclic guanosine monophosphate, which plays important roles in a variety of physiological responses such as vision, olfaction, muscle contraction, homeostatic regulation, cardiovascular and nervous function. There are two types of GCs in animals, soluble (sGCs) which are found ubiquitously in cell cytoplasm, and receptor (rGC) forms which span cell membranes. The complete genomes of several vertebrate and invertebrate species are now available. These data provide a platform to investigate the evolution of GCs across a diverse range of animal phyla. RESULTS: In this analysis we located GC genes from a broad spectrum of vertebrate and invertebrate animals and reconstructed molecular phylogenies for both sGC and rGC proteins. The most notable features of the resulting phylogenies are the number of lineage specific rGC and sGC expansions that have occurred during metazoan evolution. Among these expansions is a large nematode specific rGC clade comprising 21 genes in C. elegans alone; a vertebrate specific expansion in the natriuretic receptors GC-A and GC-B; a vertebrate specific expansion in the guanylyl GC-C receptors, an echinoderm specific expansion in the sperm rGC genes and a nematode specific sGC clade. Our phylogenetic reconstruction also shows the existence of a basal group of nitric oxide (NO) insensitive insect and nematode sGCs which are regulated by O(2). This suggests that the primordial eukaryotes probably utilized sGC as an O(2 )sensor, with the ligand specificity of sGC later switching to NO which provides a very effective local cell-to-cell signalling system. Phylogenetic analysis of the sGC and bacterial heme nitric oxide/oxygen binding protein domain supports the hypothesis that this domain originated from a cyanobacterial source. CONCLUSION: The most salient feature of our phylogenies is the number of lineage specific expansions, which have occurred within the GC gene family during metazoan evolution. Our phylogenetic analyses reveal that the rGC and sGC multi-domain proteins evolved early in eumetazoan evolution. Subsequent gene duplications, tissue specific expression patterns and lineage specific expansions resulted in the evolution of new networks of interaction and new biological functions associated with the maintenance of organismal complexity and homeostasis

Chemoreceptor genes: what can we learn from Caenorhabditis elegans and how can we apply this information to studies on other nematodes?

Soil dwelling nematodes encounter many types of volatile and water-soluble molecules in their environment. For free-living nematodes like Caenorhabdiris clegnns, successful foraging depends on the ability to detect a gradient in one odorant while ignoring extraneous odoun. The infectious stages of plant and animal parasitic nematodes also rely on chemoreception as their primary host finding cue. Using a combination of genetic, molecular and bioinformatic approaches chemoreceptor genes have been identified in C. clegans. These C. elegans chemoreceptor genes encode seven-transmembrane G-protein coupled receptors (GPCR) and comprise the largest gene family in this nematode. GPCR are also involved in olfactory signal transduction across a broad spectrum of animals including insects, crustaceans, fish and mammals, but the C. elegans (and Drosophila) chemoreceptor genes have no sequence homology to vertebrate GPCR odour receptor genes and they also differ from vertebrate odour receptor genes in their genomic structure. We review the genomic structure and diversity of odorant and chemoreceptor gene families in vertebrates and invertebrates and describe our attempts, using homology-based approaches, to isolate chemoreceptor genes in the entomopathogenic nematode Heterorhabditis bacteriophora

Chemoreceptor genes: what can we learn from Caenorhabditis elegans and how can we apply this information to studies on other nematodes?

Soil dwelling nematodes encounter many types of volatile and water-soluble molecules in their environment. For free-living nematodes like Caenorhabdiris clegnns, successful foraging depends on the ability to detect a gradient in one odorant while ignoring extraneous odoun. The infectious stages of plant and animal parasitic nematodes also rely on chemoreception as their primary host finding cue. Using a combination of genetic, molecular and bioinformatic approaches chemoreceptor genes have been identified in C. clegans. These C. elegans chemoreceptor genes encode seven-transmembrane G-protein coupled receptors (GPCR) and comprise the largest gene family in this nematode. GPCR are also involved in olfactory signal transduction across a broad spectrum of animals including insects, crustaceans, fish and mammals, but the C. elegans (and Drosophila) chemoreceptor genes have no sequence homology to vertebrate GPCR odour receptor genes and they also differ from vertebrate odour receptor genes in their genomic structure. We review the genomic structure and diversity of odorant and chemoreceptor gene families in vertebrates and invertebrates and describe our attempts, using homology-based approaches, to isolate chemoreceptor genes in the entomopathogenic nematode Heterorhabditis bacteriophora

Changes in cGMP Levels Affect the Localization of EGL-4 in AWC in Caenorhabditis elegans

The Protein Kinase G, EGL-4, is required within the C. elegans AWC sensory neurons to promote olfactory adaptation. After prolonged stimulation of these neurons, EGL-4 translocates from the cytosol to the nuclei of the AWC. This nuclear translocation event is both necessary and sufficient for adaptation of the AWC neuron to odor. A cGMP binding motif within EGL-4 and the Gα protein ODR-3 are both required for this translocation event, while loss of the guanylyl cyclase ODR-1 was shown to result in constitutively nuclear localization of EGL-4. However, the molecular changes that are integrated over time to produce a stably adapted response in the AWC are unknown. Here we show that odor-induced fluctuations in cGMP levels in the adult cilia may be responsible in part for sending EGL-4 into the AWC nucleus to produce long-term adaptation. We found that reductions in cGMP that result from mutations in the genes encoding the cilia-localized guanylyl cyclases ODR-1 and DAF-11 result in constitutively nuclear EGL-4 even in naive animals. Conversely, increases in cGMP levels that result from mutations in cGMP phosphodiesterases block EGL-4 nuclear entry even after prolonged odor exposure. Expression of a single phosphodiesterase in adult, naive animals was sufficient to modestly increase the number of animals with nuclear EGL-4. Further, coincident acute treatment of animals with odor and the phosphodiesterase inhibitor 3-isobutyl-1-methylxanthine (IBMX) decreased the number of animals with nuclear EGL-4. These data suggest that reducing cGMP levels in AWC is necessary and even partially sufficient for nuclear translocation of EGL-4 and adaptation as a result of prolonged odor exposure. Our genetic analysis and chemical treatment of C. elegans further indicate that cilia morphology, as defined by fluorescent microscopic observation of the sensory endings, may allow for odor-induced fluctuations in cGMP levels and this fluctuation may be responsible for sending EGL-4 into the AWC nucleus

Regulators of AWC-Mediated Olfactory Plasticity in Caenorhabditis elegans

While most sensory neurons will adapt to prolonged stimulation by down-regulating their responsiveness to the signal, it is not clear which events initiate long-lasting sensory adaptation. Likewise, we are just beginning to understand how the physiology of the adapted cell is altered. Caenorhabditis elegans is inherently attracted to specific odors that are sensed by the paired AWC olfactory sensory neurons. The attraction diminishes if the animal experiences these odors for a prolonged period of time in the absence of food. The AWC neuron responds acutely to odor-exposure by closing calcium channels. While odortaxis requires a Gα subunit protein, cGMP-gated channels, and guanylyl cyclases, adaptation to prolonged odor exposure requires nuclear entry of the cGMP-dependent protein kinase, EGL-4. We asked which candidate members of the olfactory signal transduction pathway promote nuclear entry of EGL-4 and which molecules might induce long-term adaptation downstream of EGL-4 nuclear entry. We found that initiation of long-term adaptation, as assessed by nuclear entry of EGL-4, is dependent on G-protein mediated signaling but is independent of fluxes in calcium levels. We show that long-term adaptation requires polyunsaturated fatty acids (PUFAs) that may act on the transient receptor potential (TRP) channel type V OSM-9 downstream of EGL-4 nuclear entry. We also present evidence that high diacylglycerol (DAG) levels block long-term adaptation without affecting EGL-4 nuclear entry. Our analysis provides a model for the process of long-term adaptation that occurs within the AWC neuron of C. elegans: G-protein signaling initiates long-lasting olfactory adaptation by promoting the nuclear entry of EGL-4, and once EGL-4 has entered the nucleus, processes such as PUFA activation of the TRP channel OSM-9 may dampen the output of the AWC neuron

Invading and expanding : range dynamics and ecological consequences of the Greater White-Toothed Shrew (Crocidura russula) invasion in Ireland

Establishing how invasive species impact upon pre-existing species is a fundamental question in ecology and conservation biology. The greater white-toothed shrew (Crocidura russula) is an invasive species in Ireland that was first recorded in 2007 and which, according to initial data, may be limiting the abundance/distribution of the pygmy shrew (Sorex minutus), previously Ireland’s only shrew species. Because of these concerns, we undertook an intensive live-trapping survey (and used other data from live-trapping, sightings and bird of prey pellets/nest inspections collected between 2006 and 2013) to model the distribution and expansion of C. russula in Ireland and its impacts on Ireland’s small mammal community. The main distribution range of C. russula was found to be approximately 7,600 km2 in 2013, with established outlier populations suggesting that the species is dispersing with human assistance within the island. The species is expanding rapidly for a small mammal, with a radial expansion rate of 5.5 km/yr overall (2008–2013), and independent estimates from live-trapping in 2012–2013 showing rates of 2.4–14.1 km/yr, 0.5–7.1 km/yr and 0–5.6 km/yr depending on the landscape features present. S. minutus is negatively associated with C. russula. S. minutus is completely absent at sites where C. russula is established and is only present at sites at the edge of and beyond the invasion range of C. russula. The speed of this invasion and the homogenous nature of the Irish landscape may mean that S. minutus has not had sufficient time to adapt to the sudden appearance of C. russula. This may mean the continued decline/disappearance of S. minutus as C. russula spreads throughout the island