Abstract In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, usingOnthophagus taurus(Schreber, 1759) and its sister speciesO. illyricus(Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called thepedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (SelfandCrossinoculation treatments, respectively). We then crossed the resulting adultO. taurusin three combinations (Selffemale XSelfmale;Selffemale XCrossmale;Crossfemale XSelfmale). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, theSelfXSelfline would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between‐partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre‐copulatory isolation as evidenced by reduced sperm transfer in theSelfXSelfline. This pattern is consistent either with microbiome‐mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.
more »
« less
Reciprocal microbiome transplants differentially rescue fitness in two syntopic dung beetle sister species (Scarabaeidae: Onthophagus )
1. Microbial symbionts play a crucial role in the development, health, and homeostasis of their hosts. However, the eco‐evolutionary conditions shaping these relationships and the evolutionary scale at which host–microbiome interactions may diverge warrant further investigation, especially in non‐model systems. This study examines the impact of reciprocal gut microbiome transplants between two ecologically very similar, sympatric, and syntopic dung beetle sister species. 2.Onthophagus vaccaandOnthophagus mediuswere specifically used to compare the growth, development, and fitness outcomes of individuals that were either (i) reared in the presence of a microbiome provided by a mother of the same species (“self‐inoculated”), (ii) forced to develop with a microbiome derived from a heterospecific mother (“cross‐inoculated”), or (iii) reared without a maternally transmitted microbiome. 3. This study found that individuals reared in the absence of a maternally derived gut microbiome incur detrimental changes in survival, as well as in several metrics signalling normative development. Furthermore, such negative effects are only partly rescued through inoculation with a heterologous microbiome. 4. Collectively, this study's results suggest that inoculation with a species‐specific, maternally transmitted microbiome is critical for normative development, that the significance of maternally derived microbiota for host survival differs across species, and that the phenotypic outcomes resulting from host–microbiome interactions may diverge even between closely related, ecologically similar host species.
more »
« less
- Award ID(s):
- 1901680
- PAR ID:
- 10450208
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecological Entomology
- Volume:
- 46
- Issue:
- 4
- ISSN:
- 0307-6946
- Format(s):
- Medium: X Size: p. 946-954
- Size(s):
- p. 946-954
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Vertebrates host complex microbiomes that impact their physiology. In many taxa, including colourful wood-warblers, gut microbiome similarity decreases with evolutionary distance. This may suggest that as host populations diverge, so do their microbiomes, because of either tight coevolutionary dynamics, or differential environmental influences, or both. Hybridization is common in wood-warblers, but the effects of evolutionary divergence on the microbiome during secondary contact are unclear. Here, we analyse gut microbiomes in two geographically disjunct hybrid zones between blue-winged warblers (Vermivora cyanoptera) and golden-winged warblers (Vermivora chrysoptera). We performed 16S faecal metabarcoding to identify species-specific bacteria and test the hypothesis that host admixture is associated with gut microbiome disruption. Species identity explained a small amount of variation between microbiomes in only one hybrid zone. Co-occurrence of species-specific bacteria was rare for admixed individuals, yet microbiome richness was similar among admixed and parental individuals. Unexpectedly, we found several bacteria that were more abundant among admixed individuals with a broader deposition of carotenoid-based plumage pigments. These bacteria are predicted to encode carotenoid biosynthesis genes, suggesting birds may take advantage of pigments produced by their gut microbiomes. Thus, host admixture may facilitate beneficial symbiotic interactions which contribute to plumage ornaments that function in sexual selection.more » « less
-
Abstract Pathogens play a key role in insect population dynamics, contributing to short‐term fluctuations in abundance as well as long‐term demographic trends. Two key factors that influence the effects of entomopathogens on herbivorous insect populations are modes of pathogen transmission and larval host plants. In this study, we examined tritrophic interactions between a sequestering specialist lepidopteran,Euphydryas phaeton, and a viral pathogen, Junonia coenia densovirus, on its native host plant,Chelone glabra, and a novel host plant,Plantago lanceolata, to explore whether host plant mediates viral transmission, survival, and viral loads. A two‐factor factorial experiment was conducted in the laboratory with natal larval clusters randomly assigned to either the native or novel host plant and crossed with either uninoculated controls or viral inoculation (20% of individuals in the cluster inoculated). Diapausing clusters were overwintered in the laboratory and checked weekly for mortality. At the end of diapause, all surviving individuals were reared to adulthood to estimate survivorship. All individuals were screened to quantify viral loads, and estimate horizontal transmission postmortem. To test for vertical transmission, adults were mated, and the progeny were screened for viral presence. Within virus‐treated groups, we found evidence for both horizontal and vertical transmission. Larval clusters reared on the native host plant had slightly higher horizontal transmission. Survival probability was lower in clusters feeding on the native host plant, with inoculated groups reared on the native host plant experiencing complete mortality. Viral loads did not differ by the host plant, although viral loads decreased with increased sequestration of secondary compounds on both host plants. Our results indicate that the use of a novel host plant may confer fitness benefits in terms of survival and reduced viral transmission when larvae feeding on it are infected with this pathogen, supporting hypotheses of potential evolutionary advantages of a host range expansion in the context of tritrophic interactions.more » « less
-
Abstract The bacterial gut microbiota of many animals is known to be important for many physiological functions including detoxification. The selective pressures imposed on insects by exposure to toxins may also be selective pressures on their symbiotic bacteria, who thus may contribute to the mechanism of toxin tolerance for the insect. Amatoxins are a class of cyclopeptide mushroom toxins that primarily act by binding to RNA polymerase II and inhibiting transcription. Several species of mycophagousDrosophilaare tolerant to amatoxins found in mushrooms of the genusAmanita, despite these toxins being lethal to most other known eukaryotes. These species can tolerate amatoxins in natural concentrations to utilize toxic mushrooms as larval hosts, but the mechanism by which these species are tolerant remains unknown. Previous data have shown that a local population ofD. tripunctataexhibits significant genetic variation in toxin tolerance. This study assesses the potential role of the microbiome in α‐amanitin tolerance in six wild‐derived strains ofDrosophila tripunctata. Normal and antibiotic‐treated samples of six strains were reared on diets with and without α‐amanitin, and then scored for survival from the larval stage to adulthood and for development time to pupation. Our results show that a substantial reduction in bacterial load does not influence toxin tolerance in this system, while confirming genotype and toxin‐specific effects on survival are independent of the microbiome composition. Thus, we conclude that this adaptation to exploit toxic mushrooms as a host is likely intrinsic to the fly's genome and not a property of their microbiome.more » « less
-
Abstract Microbial symbionts can influence their hosts in stunningly diverse ways. Emerging research suggests that an underappreciated facet of these relationships is the influence microbes can have on their host's responses to novel, or stressful, environmental conditions. We sought to address these and related questions in populations resulting from the recent introduction and subsequent rapid range expansion ofOnthophagus taurusdung beetles. Specifically, we manipulated both microbial communities and rearing temperature to detect signatures of developmental and life history differentiation in response to the local thermal conditions in two populations derived from the southern most (Florida) and northern most (Michigan) extremes of the exotic Eastern U.S. range ofO. taurus. We then sought to determine the contributions, if any, of host‐associated microbiota to this differentiation. We found that when reared under common garden conditions individuals from Florida and Michigan populations differed significantly in developmental performance measures and life history traits, consistent with population divergence. At the same time, and contrary to our predictions, we failed to find support for the hypothesis that animals perform better if reared at temperatures that match their location of origin and that performance differences may be mediated by host‐associated microbiota. Instead, we found that microbiome swapping across host populations improved developmental performance in both populations, consistent with enemy release dynamics. We discuss the implications of our results for our understanding of the rapid spread of exoticO. taurusthrough the Eastern United States and the significance of symbiosis in host responses to novel environmental conditions more broadly.more » « less
An official website of the United States government
