When night never falls : female sexual signalling in a nocturnal insect along a latitudinal gradient

The environment can play an important role in animal communication by affecting signal transmission and detection. Variation in the signalling environment is expected to be especially pronounced in widely distributed species, potentially affecting how their signals are detected. Such environmental variability is presumably relevant for sedentary females of a nocturnal capital breeder, the European common glow-worm (Lampyris noctiluca), which produce green light during the night to attract flying males to mate. Being widely distributed in Europe, glow-worm populations are exposed to both rapidly descending, darker summer nights in the south, and slowly dimming, brighter summer nights further north, with the latter potentially posing challenges to the visibility of the female glow. To test how female signalling is affected by latitude, we sampled glowing females during summer nights along a latitudinal gradient in Finland, Northern Europe, and used a novel apparatus to measure the intensity and peak wavelength (hue/colour) of their glow. Surprisingly, females at higher latitudes, similar to those at lower latitudes, were commonly glowing during the brightest (and hence the shortest) nights of the year. Females also glowed brighter in more northern areas, partly due to their larger body size, whereas the colour of their glow was not associated with latitude. Since females glow even during midsummer, independent of latitude, the increase in glow intensity at higher latitudes presumably serves to maintain signal visibility in brighter signalling conditions. Overall, these findings highlight the influence of environmental conditions on the evolution of sexual signals, especially in the context of species distribution range. Significance statement When environmental conditions impact signal transmission and perception, local conditions can have a crucial role in shaping animal communication and signal evolution. To analyse how dark-dependant common glow-worm females cope with variable nocturnal light environments, we used a novel apparatus, presumably not applied to living animals before, to measure female glow intensity at various latitudes along a latitudinal gradient. Interestingly, females did not avoid signalling during the brightest summer nights, but instead, their glow intensity and body size both increased with latitude. These findings suggest that females can ensure visibility to mate-searching males over a range of local conditions. Our study therefore shows how females can adapt to environmental constraints on signal visibility, and how the expression of sexual signals is shaped not only by social interactions but also by the signalling environment.Peer reviewe

The role of ocelli in cockroach optomotor performance

Insect ocelli are relatively simple eyes that have been assigned various functions not related to pictorial vision. In some species they function as sensors of ambient light intensity, from which information is relayed to various parts of the nervous system, e.g., for the control of circadian rhythms. In this work we have investigated the possibility that the ocellar light stimulation changes the properties of the optomotor performance of the cockroach Periplaneta americana. We used a virtual reality environment where a panoramic moving image is presented to the cockroach while its movements are recorded with a trackball. Previously we have shown that the optomotor reaction of the cockroach persists down to the intensity of moonless night sky, equivalent to less than 0.1 photons/s being absorbed by each compound eye photoreceptor. By occluding the compound eyes, the ocelli, or both, we show that the ocellar stimulation can change the intensity dependence of the optomotor reaction, indicating involvement of the ocellar visual system in the information processing of movement. We also measured the cuticular transmission, which, although relatively large, is unlikely to contribute profoundly to ocellar function, but may be significant in determining the mean activity level of completely blinded cockroaches

Behavioral responses to visual overstimulation in the cockroach Periplaneta americana L.

Abstract In the visual systems of insects, different types of photoreceptors contribute to specialized visual channels that mediate distinct functions and behaviors. Large compound eyes of Periplaneta americana contain photoreceptors of two spectral classes, broadband green-sensitive photoreceptors and narrow-band UV-sensitive photoreceptors. Here, we investigated how visual stimulation by UV and green light affects locomotor, resting, and grooming behaviors in P. americana under conditions when light avoidance is not possible. We show that green but not UV light stimulates locomotor activity, inducing paradoxical positive masking. Duration of resting and grooming decreased with increasing light intensity, consistent with development of behavioral stress in response to visual overstimulation. A reaction of full immobility is described under UV light and at higher intensities of green light, with relative periods of immobility and grooming strongly negatively correlated. Low-intensity UV was more effective than low-intensity green light in suppressing grooming and inducing immobility. Our results suggest that locomotor activity in P. americana is mainly regulated by green-sensitive photoreceptors, and that dim UV light can trigger behavioral immobility, whereas both wavelengths induce stress-like reactions at high intensities. Considering the intrinsic UV sensitivity of green-sensitive photoreceptors, the contrasting behavioral responses indicate antagonistic interactions between UV and green visual channels

When night never falls:female sexual signalling in a nocturnal insect along a latitudinal gradient

Abstract The environment can play an important role in animal communication by affecting signal transmission and detection. Variation in the signalling environment is expected to be especially pronounced in widely distributed species, potentially affecting how their signals are detected. Such environmental variability is presumably relevant for sedentary females of a nocturnal capital breeder, the European common glow-worm (Lampyris noctiluca), which produce green light during the night to attract flying males to mate. Being widely distributed in Europe, glow-worm populations are exposed to both rapidly descending, darker summer nights in the south, and slowly dimming, brighter summer nights further north, with the latter potentially posing challenges to the visibility of the female glow. To test how female signalling is affected by latitude, we sampled glowing females during summer nights along a latitudinal gradient in Finland, Northern Europe, and used a novel apparatus to measure the intensity and peak wavelength (hue/colour) of their glow. Surprisingly, females at higher latitudes, similar to those at lower latitudes, were commonly glowing during the brightest (and hence the shortest) nights of the year. Females also glowed brighter in more northern areas, partly due to their larger body size, whereas the colour of their glow was not associated with latitude. Since females glow even during midsummer, independent of latitude, the increase in glow intensity at higher latitudes presumably serves to maintain signal visibility in brighter signalling conditions. Overall, these findings highlight the influence of environmental conditions on the evolution of sexual signals, especially in the context of species distribution range

Phenotypic plasticity in Periplaneta americana photoreceptors

Abstract Plasticity is a crucial aspect of neuronal physiology essential for proper development and continuous functional optimization of neurons and neural circuits. Despite extensive studies of different visual systems, little is known about plasticity in mature microvillar photoreceptors. Here we investigate changes in electrophysiological properties and gene expression in photoreceptors of the adult cockroach, Periplaneta americana, after exposure to constant light (CL) or constant dark (CD) for several months. After CL, we observed a decrease in mean whole-cell capacitance, a proxy for cell membrane area, from 362 ± 160 to 157 ± 58 pF, and a decrease in absolute sensitivity. However, after CD, we observed an increase in capacitance to 561 ± 155 pF and an increase in absolute sensitivity. Small changes in the expression of light-sensitive channels and signaling molecules were detected in CD retinas, together with a substantial increase in the expression of the primary green-sensitive opsin (GO1). Accordingly, light-induced currents became larger in CD photoreceptors. Even though normal levels of GO1 expression were retained in CL photoreceptors, light-induced currents became much smaller, suggesting that factors other than opsin are involved. Latency of phototransduction also decreased significantly in CL photoreceptors. Sustained voltage-activated K+ conductance was not significantly different between the experimental groups. The reduced capacitance of CL photoreceptors expanded their bandwidth, increasing the light-driven voltage signal at high frequencies. However, voltage noise was also amplified, probably because of unaltered expression of TRPL channels. Consequently, information transfer rates were lower in CL than in control or CD photoreceptors. These changes in whole-cell capacitance and electrophysiological parameters suggest that structural modifications can occur in the photoreceptors to adapt their function to altered environmental conditions. The opposing patterns of modifications in CL and CD photoreceptors differ profoundly from previous findings in Drosophila melanogaster photoreceptors

Electrical interactions between photoreceptors in the compound eye of Periplaneta americana

Abstract The compound eye of Periplaneta americana contains two spectral classes of photoreceptors: narrow-band UV-sensitive and broad-band green-sensitive. In intracellular recordings, stimulation of green-sensitive photoreceptors with flashes of relatively bright UV/violet light produced anomalous delayed depolarization after the end of the normal light response, whereas stimulation of UV-sensitive photoreceptors with green light elicited biphasic responses characterized by initial transient hyperpolarization followed by prolonged delayed depolarization. To explore the basis for these findings, we used RNA interference to selectively suppress expression of the genes encoding green opsin (GO1), UV opsin (UVO) or both. The hyperpolarizing component in UV-sensitive photoreceptors was eliminated and the delayed depolarization was reduced after GO1 knockdown, suggesting that the hyperpolarization represents fast inhibitory interactions between green- and UV-sensitive photoreceptors. Green-sensitive photoreceptor responses of GO1 knockdowns to flashes of UV/violet were almost exclusively biphasic, whereas residual responses to green had normal kinetics. Knockdown of UVO reduced the responses of UV-sensitive photoreceptors but had minor effects on delayed depolarization in green-sensitive photoreceptors. Angular sensitivity analysis indicated that delayed depolarization of green-sensitive photoreceptors by violet light originates from excitation of (an)other photoreceptor(s) in the same ommatidium. The angle at which the maximal delayed depolarization was observed in green-sensitive photoreceptors stimulated with violet light did not match the angle of the maximal transient depolarization. In contrast, no significant mismatch was observed for delayed depolarization elicited by green light. These results suggest that the cellular sources of the normal transient and additional delayed depolarization by violet light are separate and distinct

Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

Abstract Absence of screening pigment in insect compound eyes has been linked to visual dysfunction. We investigated how its loss in a white-eyed mutant (W-E) alters the photoreceptor electrophysiological properties, opsin gene expression, and the behavior of the cockroach, Periplaneta americana. Whole-cell patch-clamp recordings of green-sensitive photoreceptors in W-E cockroaches gave reduced membrane capacitance, absolute sensitivity to light, and light-induced currents. Decreased low-pass filtering increased voltage-bump amplitudes in W-E photoreceptors. Intracellular recordings showed that angular sensitivity of W-E photoreceptors had two distinct components: a large narrow component with the same acceptance angle as wild type, plus a relatively small wide component. Information processing was evaluated using Gaussian white-noise modulated light stimulation. In bright light, W-E photoreceptors demonstrated higher signal gain and signal power than wild-type photoreceptors. Expression levels of the primary UV- and green-sensitive opsins were lower and the secondary green-sensitive opsin significantly higher in W-E than in wild-type retinae. In behavioral experiments, W-E cockroaches were significantly less active in dim green light, consistent with the relatively low light sensitivity of their photoreceptors. Overall, these differences can be related to the loss of screening pigment function and to a compensatory decrease in the rhabdomere size in W-E retinae

Inhibition of endogenous nitric oxide in the heart enhances matrix metalloproteinase-2 release

1. Matrix metalloproteinase (MMP) activity is upregulated in pathologies such as atherosclerosis during which endogenous nitric oxide (NO) biosynthesis is reduced. Diminished levels of NO, an antioxidant species, may result in higher oxidative stress. Oxidants are capable of activating MMPs from their zymogen forms. We examined whether basal biosynthesis of NO in the coronary circulation regulates MMP-2 activity. 2. In isolated rat hearts perfused with Krebs–Henseleit buffer at a constant flow of 10 ml min(−1), we measured the release of MMP-2 into the coronary effluent by gelatin zymography. The main gelatinolytic activity of 72-kDa corresponds to MMP-2. Infusion of the NO synthase inhibitor N(G)-nitro-L-arginine methyl ester (L-NAME) concentration dependently increased coronary perfusion pressure (CPP) (by 48±11 mmHg with 100 μM) and enhanced the release of the 72-kDa MMP-2 in the effluent. Coinfusion of the NO donor S-nitroso-N-acetyl-D,L-penicillamine (SNAP, 1 μM) with L-NAME abolished both the increase in CPP and the enhanced MMP-2 release. 3. The thromboxane A(2) mimetic U46619 increased CPP to the same extent as L-NAME without increasing 72-kDa activity in the effluent, suggesting that MMP-2 release is not caused simply by enhanced perfusion pressure. 4. Infusion of either L-NAME or U46619 did not significantly enhance LDH release. 5. L-NAME infusion concentration dependently increased the level of lipid hydroperoxides in homogenates prepared from the perfused hearts. Coinfusion of SNAP prevented this increase. 6. These data reveal another cytoprotective mechanism of endogenous NO biosynthesis in the heart, the inhibition of MMP-2 release

Distinct roles of light-activated channels TRP and TRPL in photoreceptors of periplaneta americana

Electrophysiological studies in Drosophila melanogaster and Periplaneta americana have found that the receptor current in their microvillar photoreceptors is generated by two light-activated cationic channels, TRP (transient receptor potential) and TRPL (TRP-like), each having distinct properties. However, the relative contribution of the two channel types to sensory information coding by photoreceptors remains unclear. We recently showed that, in contrast to the diurnal Drosophila in which TRP is the principal phototransduction channel, photoreceptors of the nocturnal P americana strongly depend on TRPL. Here, we perform a functional analysis, using patch-clamp and intracellular recordings, of P americana photoreceptors after RNA interference to knock down TRP (TRPkd) and TRPL (TRPLkd). Several functional properties were changed in both knockdown phenotypes: Cell membrane capacitance was reduced 1.7-fold, light sensitivity was greatly reduced, and amplitudes of sustained light-induced currents and voltage responses decreased more than twofold over the entire range of light intensities. The information rate (IR) was tested using a Gaussian white-noise modulated light stimulus and was lower in TRPkd photoreceptors (28 ± 21 bits/s) than in controls (52 ± 13 bits/s) because of high levels of bump noise. In contrast, although signal amplitudes were smaller than in controls, the mean IR of TRPLkd photoreceptors was unchanged at 54 ± 29 bits/s1 because of proportionally lower noise. We conclude that TRPL channels provide high-gain/high-noise transduction, suitable for vision in dim light, whereas transduction by TRP channels is relatively low-gain/low-noise and allows better information transfer in bright light