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, 281 (1774), 20132582

Anatomical and Functional Analysis of Domestication Effects on the Olfactory System of the Silkmoth Bombyx Mori

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Anatomical and Functional Analysis of Domestication Effects on the Olfactory System of the Silkmoth Bombyx Mori

Sonja Bisch-Knaden et al. Proc Biol Sci.

Abstract

The silkmoth Bombyx mori is the main producer of silk worldwide and has furthermore become a model organism in biological research, especially concerning chemical communication. However, the impact domestication might have had on the silkmoth's olfactory sense has not yet been investigated. Here, we show that the pheromone detection system in B. mori males when compared with their wild ancestors Bombyx mandarina seems to have been preserved, while the perception of environmental odorants in both sexes of domesticated silkmoths has been degraded. In females, this physiological impairment was mirrored by a clear reduction in olfactory sensillum numbers. Neurophysiological experiments with hybrids between wild and domesticated silkmoths suggest that the female W sex chromosome, so far known to have the sole function of determining femaleness, might be involved in the detection of environmental odorants. Moreover, the coding of odorants in the brain, which is usually similar among closely related moths, differs strikingly between B. mori and B. mandarina females. These results indicate that domestication has had a strong impact on odour detection and processing in the olfactory model species B. mori.

Keywords: Bombyx mandarina; Bombyx mori; W chromosome; domestication; olfactory coding; olfactory sensilla.

Figures

Figure 1.
Figure 1.
Antennal morphology is preserved in domesticated males but not in females. (a) Wild silkmoths B. mandarina, domesticated silkmoths B. mori and hybrids of both were studied. (b) Schematic of a silkmoth's head with its left antenna; the bold line represents the antennal stem; thin lines perpendicular to the stem denote branches. The black frame marks the middle branch where olfactory sensilla were counted. (c) Close-up view of long trichoids (arrowheads) and sensilla basiconica (arrows) of a female B. mori; scale bar, 2 µm. (d) Frequency of olfactory sensilla on the middle antennal branch of males (solid line) and females (dotted line); size ranges of medium-length trichoids and sensilla basiconica broadly overlap [2], so the numbers of these two sensillum types were pooled. The middle antennal branch was chosen because sensillum numbers and their ratios are constant in the middle region of the antenna of B. mori, irrespective of the size of the animal [2]. Symbols represent data from individual silkmoths; the diagonal separates animals that have more long trichoids than sensilla basiconica and medium-length trichoids (above the diagonal) from animals with the reverse sensillum ratio (below the diagonal). The sensillum ratios for B. mori are in accordance with ratios from data based on an estimation of sensillum numbers of the whole antenna [2]. (e) Detail of a middle antennal branch of a B. mandarina female (i) and a B. mori female (ii); scale bar, 20 µm.
Figure 2.
Figure 2.
Plant responses but not pheromone responses are affected by domestication. (a) Example EAG recordings from the clipped antennae of a B. mandarina male; stimulus duration (black horizontal bar) was 0.5 s. (b) Pheromone responses are shown as a multiple of the response to the solvent hexane (see the electronic supplementary material, data file). Solvent responses were similar between the species; B. mandarina: 0.218 mV ± 0.202 mV, B. mori: 0.219 mV ± 0.124 mV; p = 0.99, t-test. Pheromone concentrations were chosen to elicit similar amplitudes for both compounds [16]. Bars show mean normalized EAG amplitudes; error bars represent s.d. All pheromone responses are different from responses to the solvent (p < 0.05, paired t-test). Values for wild and domesticated silkmoths did not differ (p > 0.05, t-test). (c–f) Electro-antennogram recordings after stimulation with 14 environmental odorants. (c) Responses of wild and domesticated males, (d) wild and domesticated females, (e) hybrid males, (f) hybrid females are shown as a multiple of the response to the solvent (see the electronic supplementary material, data file). Odorants were diluted in mineral oil (1 : 103, 4.9–7.3 µg on filter paper); stimulus duration was 0.5 s. Open bars represent values that were not different from the solvent response (p > 0.05, paired t-test). Responses to the solvent were similar between species; B. mandarina male: 0.046 mV ± 0.029 mV, B. mori male: 0.046 mV ± 0.008 mV; p = 0.98; B. mandarina female: 0.031 mV ± 0.010 mV, B. mori female: 0.035 mV ± 0.020 mV; p = 0.56, t-test. For each odorant, asterisks mark significant differences between species; *p < 0.05, **p < 0.01, ***p < 0.001, t-test. (g) Dendrogram of silkmoths according to their mean EAG amplitudes; hierarchical cluster analysis using Ward's minimum variance method. The origin of the sex chromosomes is shown next to the symbol of the respective species (red, from wild silkmoths; blue, from domesticated silkmoths).
Figure 3.
Figure 3.
Odour-evoked neural activity patterns in the brain are altered in domesticated females. (a) Frontal view of the left antennal lobe; the antennal nerve enters from the top right corner; scale bar, 100 µm. Mean antennal lobe volumes differed between wild (n = 5) and domesticated (n = 5) females; error bars represent s.d.; **p < 0.01, t-test; (b) Example results of calcium imaging recordings after a 2 s odour stimulation. The odour-evoked increase of fluorescence is colour-coded (see scale) and superimposed onto the view of the left antennal lobe; the entrance of the antennal nerve points upwards; r, correlation coefficient between neural activity patterns; scale bar, 200 µm; the white checked grid was added for better orientation. (c) Distribution of individual wild (n = 7) and domesticated (n = 12) females based on their neural responses evoked by 14 environmental odorants (same as in figure 2c–f). Correlations between all possible pairwise combinations of odorants (n = 91 comparisons) were used for this principle component analysis. The first three principal components (PCs) are shown; values in parentheses depict the proportion of the observed variance in the data that was explained by PC1, PC2 and PC3. Neural response similarities differ between wild and domesticated females (p = 0.005, ANOSIM). (d) Dendrogram of individual females (n = 57) from six insect species based on results from calcium imaging recordings (n = 91 correlations per animal; see the electronic supplementary material, data file); hierarchical cluster analysis using Ward's method; dotted line, automatic truncation. Silhouettes of the insects are drawn proportionally.

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