The olfactory basis of orchid pollination by mosquitoes.

Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the mosquito brain. Here we show that Aedes spp. mosquitoes, including Aedes aegypti, are effective pollinators of the Platanthera obtusata orchid, and demonstrate this mutualism is mediated by the orchid's scent and the balance of excitation and inhibition in the mosquito's antennal lobe (AL). The P. obtusata orchid emits an attractive, nonanal-rich scent, whereas related Platanthera species-not visited by mosquitoes-emit scents dominated by lilac aldehyde. Calcium imaging experiments in the mosquito AL revealed that nonanal and lilac aldehyde each respectively activate the LC2 and AM2 glomerulus, and remarkably, the AM2 glomerulus is also sensitive to N,N-diethyl-meta-toluamide (DEET), a mosquito repellent. Lateral inhibition between these 2 glomeruli reflects the level of attraction to the orchid scents. Whereas the enriched nonanal scent of P. obtusata activates the LC2 and suppresses AM2, the high level of lilac aldehyde in the other orchid scents inverts this pattern of glomerular activity, and behavioral attraction is lost. These results demonstrate the ecological importance of mosquitoes beyond operating as disease vectors and open the door toward understanding the neural basis of mosquito nectar-seeking behaviors.

Olfactory Preferences of the Parasitic Nematode Howardula aoronymphium and its Insect Host Drosophila falleni.

Many parasitic nematodes have an environmental infective stage that searches for hosts. Olfaction plays an important role in this process, with nematodes navigating their environment using host-emitted and environmental olfactory cues. The interactions between parasitic nematodes and their hosts are also influenced by the olfactory behaviors of the host, since host olfactory preferences drive behaviors that may facilitate or impede parasitic infection. However, how olfaction shapes parasite-host interactions is poorly understood. Here we investigated this question using the insect-parasitic nematode Howardula aoronymphium and its host, the mushroom fly Drosophila falleni. We found that both H. aoronymphium and D. falleni are attracted to mushroom odor and a subset of mushroom-derived odorants, but they have divergent olfactory preferences that are tuned to different mushroom odorants despite their shared mushroom environment. H. aoronymphium and D. falleni respond more narrowly to odorants than Caenorhabditis elegans and Drosophila melanogaster, consistent with their more specialized niches. Infection of D. falleni with H. aoronymphium alters its olfactory preferences, rendering it more narrowly tuned to mushroom odor. Our results establish H. aoronymphium-D. falleni as a model system for studying olfaction in the context of parasite-host interactions.

Diverse host-seeking behaviors of skin-penetrating nematodes.

Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are responsible for some of the most common neglected tropical diseases. The infective larvae of skin-penetrating nematodes are thought to search for hosts using sensory cues, yet their host-seeking behavior is poorly understood. We conducted an in-depth analysis of host seeking in the skin-penetrating human parasite Strongyloides stercoralis, and compared its behavior to that of other parasitic nematodes. We found that Str. stercoralis is highly mobile relative to other parasitic nematodes and uses a cruising strategy for finding hosts. Str. stercoralis shows robust attraction to a diverse array of human skin and sweat odorants, most of which are known mosquito attractants. Olfactory preferences of Str. stercoralis vary across life stages, suggesting a mechanism by which host seeking is limited to infective larvae. A comparison of odor-driven behavior in Str. stercoralis and six other nematode species revealed that parasite olfactory preferences reflect host specificity rather than phylogeny, suggesting an important role for olfaction in host selection. Our results may enable the development of new strategies for combating harmful nematode infections.

O2-sensing neurons control CO2 response in C. elegans.

Sensory behaviors are often flexible, allowing animals to generate context-appropriate responses to changing environmental conditions. To investigate the neural basis of behavioral flexibility, we examined the regulation of carbon dioxide (CO2) response in the nematode Caenorhabditis elegans. CO2 is a critical sensory cue for many animals, mediating responses to food, conspecifics, predators, and hosts (Scott, 2011; Buehlmann et al., 2012; Chaisson and Hallem, 2012). In C. elegans, CO2 response is regulated by the polymorphic neuropeptide receptor NPR-1: animals with the N2 allele of npr-1 avoid CO2, whereas animals with the Hawaiian (HW) allele or an npr-1 loss-of-function (lf) mutation appear virtually insensitive to CO2 (Hallem and Sternberg, 2008; McGrath et al., 2009). Here we show that ablating the oxygen (O2)-sensing URX neurons in npr-1(lf) mutants restores CO2 avoidance, suggesting that NPR-1 enables CO2 avoidance by inhibiting URX neurons. URX was previously shown to be activated by increases in ambient O2 (Persson et al., 2009; Zimmer et al., 2009; Busch et al., 2012). We find that, in npr-1(lf) mutants, O2-induced activation of URX inhibits CO2 avoidance. Moreover, both HW and npr-1(lf) animals avoid CO2 under low O2 conditions, when URX is inactive. Our results demonstrate that CO2 response is determined by the activity of O2-sensing neurons and suggest that O2-dependent regulation of CO2 avoidance is likely to be an ecologically relevant mechanism by which nematodes navigate gas gradients.