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Evolutionary Relationship Between Platycerus Stag Beetles and Their Mycangium-Associated Yeast Symbionts.

ABSTRACT: Adult females of stag beetles (Coleoptera: Lucanidae) possess an ovipositor-associated mycangium for conveying symbiotic microorganisms. In most lucanid species, their mycangium contains yeast symbionts of the genus Scheffersomyces Kurtzman and Suzuki that are known for their xylose-fermenting capability. The lucanid genus Platycerus Geoffroy, 1762 is a group of small blue stag beetles, in which ten Japanese species constitute a monophyletic clade. Here we examined the evolutionary relationships of these Japanese Platycerus species and their yeast symbionts, together with a Korean Platycerus species and other lucanid species as outgroup taxa. Based on the internal transcribed spacer (ITS) and the intergenic spacer (IGS) sequences, the yeast symbionts of all Platycerus species were closely related to each other and formed a monophyletic clade. There is no variation in ITS sequences of the yeast symbionts of the Japanese Platycerus species. Based on IGS sequences, the yeast symbionts formed clusters that largely reflected the geographic distribution of the host insects, being shared by sympatric Platycerus species except for P. delicatulus Lewis, 1883 and P. viridicuprus Kubota & Otobe, The symbiont phylogeny was globally not congruent with the host COI-based phylogeny, although some local congruences were observed. Statistically significant correlations were detected between the genetic distances of COI sequences of the host insects and those of IGS sequences of the yeast symbionts in Japan. These results suggest that, at least to some extent, the host insects and the yeast symbionts may have experienced co-evolutionary associations. While the Japanese Platycerus species formed a monophyletic clade in the COI phylogeny, the yeast symbionts of Japanese P. viridicuprus were very closely related to those of Korean P. hongwonpyoi Imura & Choe, 1989, suggesting the possibility that a recent secondary contact of the two beetle species during a marine withdrawal, e.g., in the last glacial period, might have resulted in an inter-specific horizontal transmission of the yeast symbiont.

SUBMITTER: Kubota K

PROVIDER: S-EPMC7338584 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Evolutionary Relationship Between Platycerus Stag Beetles and Their Mycangium-Associated Yeast Symbionts.

Kubota Kôhei K Watanabe Kana K Zhu Xue-Jiao XJ Kawakami Kako K Tanahashi Masahiko M Fukatsu Takema T

Frontiers in microbiology 20200630

Adult females of stag beetles (Coleoptera: Lucanidae) possess an ovipositor-associated mycangium for conveying symbiotic microorganisms. In most lucanid species, their mycangium contains yeast symbionts of the genus Scheffersomyces Kurtzman and Suzuki that are known for their xylose-fermenting capability. The lucanid genus Platycerus Geoffroy, 1762 is a group of small blue stag beetles, in which ten Japanese species constitute a monophyletic clade. Here we examined the evolutionary ...[more]

PMID: 32695086

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Project description:The genus Platycerus (Coleoptera: Lucanidae) is a small stag beetle group, which is adapted to cool-temperate deciduous broad-leaved forests in East Asia. Ten Platycerus species in Japan form a monophyletic clade endemic to Japan and inhabit species-specific climatic zones. They are reported to have co-evolutionary associations with their yeast symbionts of the genus Sheffersomyces based on host cytochrome oxidase subunit I (COI) and yeast intergenic spacer (IGS) phylogenies. Here we examined the heat tolerances of the yeast colonies isolated from the mycangia of 37 females belonging ten Japanese Platycerus species. The upper limits of growth and survival temperatures of each colony were decided by cultivating it at ten temperature levels between 17.5 and 40°C. Although both temperatures varied during 25.0-31.25°C, the maximum survival temperatures (MSTs) were a little higher than the maximum growth temperatures (MGTs) in 16 colonies. Pearson's correlations between these temperatures and environmental factors (elevation and 19 bioclimatic variables from Worldclim database) of host beetle collection sites were calculated. These temperatures were significantly correlated with elevation negatively, the maximum temperature of the warmest month (Bio5) positively, and some precipitative variables, especially in the warm season (Bio12, 13, 16, 18) negatively. Sympatric Platycerus kawadai and Platycerus albisomni share the same lineage of yeast symbionts that exhibit the same heat tolerance, but the elevational lower range limit of P. kawadai is higher than that of P. albisomni. Based on the field survey in their sympatric site, the maximum temperature of host wood of P. kawadai larvae is higher about 2-3°C than that of P. albisomni larvae in the summer, which may restrict the elevational range of P. kawadai to higher area. In conclusion, it is suggested that the heat tolerance of yeast symbionts restricts the habitat range of their host Platycerus species or/and that the environmental condition that host Platycerus species prefers affect the heat tolerance of its yeast symbionts.

Project description:Yeasts play an important role in the biology of the fruit fly, Drosophila melanogaster. In addition to being a valuable source of nutrition, yeasts affect D. melanogaster behavior and interact with the host immune system. Most experiments investigating the role of yeasts in D. melanogaster biology use the baker's yeast, Saccharomyces cerevisiae. However, S. cerevisiae is rarely found with natural populations of D. melanogaster or other Drosophila species. Moreover, the strain of S. cerevisiae used most often in D. melanogaster experiments is a commercially and industrially important strain that, to the best of our knowledge, was not isolated from flies. Since disrupting natural host-microbe interactions can have profound effects on host biology, the results from D. melanogaster-S. cerevisiae laboratory experiments may not be fully representative of host-microbe interactions in nature. In this study, we explore the D. melanogaster-yeast relationship using five different strains of yeast that were isolated from wild Drosophila populations. Ingested live yeasts have variable persistence in the D. melanogaster gastrointestinal tract. For example, Hanseniaspora occidentalis persists relative to S. cerevisiae, while Brettanomyces naardenensis is removed. Despite these differences in persistence relative to S. cerevisiae, we find that all yeasts decrease in total abundance over time. Reactive oxygen species (ROS) are an important component of the D. melanogaster anti-microbial response and can inhibit S. cerevisiae growth in the intestine. To determine if sensitivity to ROS explains the differences in yeast persistence, we measured yeast growth in the presence and absence of hydrogen peroxide. We find that B. naardenesis is completely inhibited by hydrogen peroxide, while H. occidentalis is not, which is consistent with yeast sensitivity to ROS affecting persistence within the D. melanogaster gastrointestinal tract. We also compared the feeding preference of D. melanogaster when given the choice between a naturally associated yeast and S. cerevisiae. We do not find a correlation between preferred yeasts and those that persist in the intestine. Notably, in no instances is S. cerevisiae preferred over the naturally associated strains. Overall, our results show that D. melanogaster-yeast interactions are more complex than might be revealed in experiments that use only S. cerevisiae. We propose that future research utilize other yeasts, and especially those that are naturally associated with Drosophila, to more fully understand the role of yeasts in Drosophila biology. Since the genetic basis of host-microbe interactions is shared across taxa and since many of these genes are initially discovered in D. melanogaster, a more realistic fly-yeast model system will benefit our understanding of host-microbe interactions throughout the animal kingdom.

Project description:Sexual dimorphisms in trait expression are widespread among animals and are especially pronounced in ornaments and weapons of sexual selection, which can attain exaggerated sizes. Expression of exaggerated traits is usually male-specific and nutrition sensitive. Consequently, the developmental mechanisms generating sexually dimorphic growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures. Yet we know little about how either of these mechanisms work, much less how they might interact with each other. We investigated the developmental mechanisms of sex-specific mandible growth in the stag beetle Cyclommatus metallifer, focusing on doublesex gene function and its interaction with juvenile hormone (JH) signaling. doublesex genes encode transcription factors that orchestrate male and female specific trait development, and JH acts as a mediator between nutrition and mandible growth. We found that the Cmdsx gene regulates sex differentiation in the stag beetle. Knockdown of Cmdsx by RNA-interference in both males and females produced intersex phenotypes, indicating a role for Cmdsx in sex-specific trait growth. By combining knockdown of Cmdsx with JH treatment, we showed that female-specific splice variants of Cmdsx contribute to the insensitivity of female mandibles to JH: knockdown of Cmdsx reversed this pattern, so that mandibles in knockdown females were stimulated to grow by JH treatment. In contrast, mandibles in knockdown males retained some sensitivity to JH, though mandibles in these individuals did not attain the full sizes of wild type males. We suggest that moderate JH sensitivity of mandibular cells may be the default developmental state for both sexes, with sex-specific Dsx protein decreasing sensitivity in females, and increasing it in males. This study is the first to demonstrate a causal link between the sex determination and JH signaling pathways, which clearly interact to determine the developmental fates and final sizes of nutrition-dependent secondary-sexual characters.

Dataset Information

Evolutionary Relationship Between Platycerus Stag Beetles and Their Mycangium-Associated Yeast Symbionts.

Publications

Evolutionary Relationship Between <i>Platycerus</i> Stag Beetles and Their Mycangium-Associated Yeast Symbionts.

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