Bactrocera oleae, Ceratitis capitata, Drosophila melanogaster, Drosophila paulistorum, Enterobacter, Horizontal exchange of microbiota, Kittiwake, Klebsiella oxytoca, Lactobacillus plantarum, Mating preference, Mediterranean fruit fly, Olive fly, Progeny, Reticulitermes flavipes, Sterile Insect Technique (SIT), Termite, Wolbachia, Zootermopsis angusticollis
In other words, do microbiota dictate host mating preference? Let’s flesh out the premise and then explore if there’s any supporting data.
If microbiota dictate mating preference, they likely have two somewhat overlapping goals. Evolution predicates that we explore such associations through the lens of the question, what’s in it for the selecting agents, i.e., the microbes?
- One, to enhance likelihood of progeny from such matings, which would ensure future bodies to colonize. In other words, vertical transmission of microbiota from one generation to the next. This is a plausible approach since natural selection manifests its effects over generational time after all. However, in order for microbiota to even have embarked on such an evolutionary journey, they’d have had to become dependent on their hosts. In doing so, host-microbe fates become forever intertwined. If host becomes extinct so do such microbes. Thus, a direct selection pressure on specific host-microbe interactions.
- If microbiota dictate mating preference without investing in the outcome of future progeny, another way to maximize their social transmission, i.e., to spread from one body to many across a generation, is by influencing another social behavior, namely virility.
Thus, the premise of microbiota dictating mating preference boils down to their making a Faustian bargain with their host to ensure or maximize likelihood of either host progeny, i.e., pass onto future host generations, or host virility, i.e., pass on to many hosts in the present generation.
Is there any data to support the idea that microbiota influence host mating preference? Yes, not in humans as yet but plenty in insects.
Experimental Data for microbiota influence on mating preference
I. Microbiota can influence fruit fly mating preference
- One of the most spectacular and compelling examples comes from that staple of genetic studies, namely, the fruit fly, Drosophila melanogaster. Relatively simple experiment.
- Separate a fruit fly population into two groups.
- Grow fruit flies in either molasses (standard cornmeal-molasses-yeast, CMY, medium) or starch for several successive generations.
- Then mix them together.
- Fruit flies grown on either molasses or starch medium for 11 generations showed homogamic mating preference.
- ‘Molasses flies‘ preferred to mate with each other. ‘Starch flies‘ also preferred to mate with each other (see figures below from 1 on experiment design and results).
- Proof that microbes were involved? Antibiotic Rx abolished mating preference.
- Fruit flies were grown on media supplemented with antibacterials, rifampicin, streptomycin, tetracycline, either together or separately.
- 10 independent experiments yielded random mating preferences, 267 homogamic and 263 heterogamic.
- Subsequent studies showed that starch medium was associated with Lactobacillus plantarum.
- Flies reared on these two different media also had different cuticular hydrocarbons, i.e., sex pheromones.
II. Microbiota were shown to influence termite reproductive fitness
- In one study, two termite species, Zootermopsis angusticollis and Reticulitermes flavipes, were fed the antibiotic, rifampicin, at the initial stages of colony formation.
- This had a lasting effect on both the gut bacterial and protozoan diversity, permanent in the former and transient in the latter.
- Effect on reproduction?
- The queen’s egg-laying capacity (oviposition) was reduced.
- This delayed colony growth and reduced colony fitness (see figures below from 2).
- Over time, termite colony population would be skewed and dominated by microbe-replete termites at the expense of relatively microbe-deficient termites.
III. Microbiota were shown to influence olive fly reproductive fitness
- In one study, egg-producing capacity of olive flies, Bactrocera oleae, was found to be dependent on the essential amino acids supplied by their gut microbes.
- Egg production in flies grown on standard diet was unaffected by antibiotic Rx.
- Egg production in flies grown on diet lacking essential amino acids was dramatically reduced by antibiotic Rx (see figure below from 3).
- Again implication is similar to the termite example, i.e., over time microbe-replete flies would take over from the relatively microbe-deficient ones.
IV. Pest control techniques inadvertently uncovered a role for microbiota in male insect virility
- The Sterile Insect Technique (SIT) (4, 5) is an important method for biological control of insects considered to be pests. In this procedure, millions of sterile male insects are reared in factories and released into the wild. The idea is that such sterile males would compete with wild-type males and since their matings would be non-productive, over time, pest populations would decline. As it turns out, such systems provide compelling data for a role of microbiota in enhancing insect virility.
- One of the drawbacks of SIT is that the methods used to sterilize male insects, for e.g., gamma radiation, also render them less competent in attracting and mating with wild-type females.
- Researching reasons why led scientists to how insect microbiota could influence their reproductive fitness.
- For e.g., in the Mediterranean fruit fly, Ceratitis capitata, adding the bacterial species, Klebsiella oxytoca, to the diet of irradiated male flies substantially improved their performance in copulatory tests (6, 7, 8, 9).
- Similar effect of enhancement of sterile male fruit flies’ ability to attract and copulate with wild-type females was observed when irradiated males were fed probiotics containing Enterobacter species (10).
- How could these bacteria influence reproductive behavior in these insects to such an extent? Possibilities include
- Chemical, i.e., pheromones.
- Behavioral, i.e., courtship rituals.
- Or combination of any of these.
Natural examples for microbiota influence on mating preference
I. In Insects
- Wolbachia is a bacterial symbiont of arthropods and nematodes (11,12, 13).
- It’s estimated to infect >50% of insect species (14).
- Wolbachia is horizontally transmitted, i.e., from adult to adult of the same species.
- It’s also vertically transmitted through the egg cytoplasm (12, 13).
- So how does Wolbachia influence mating?
- Since Wolbachia is a cytoplasmically inherited endosymbiont, it can cause reproductive isolation by inducing cytoplasmic incompatibility (CI) (15).
- If an infected female mates with an uninfected/infected male, progeny results.
- If an uninfected female mates with an infected male, embryos dies.
- Turns out only eggs, not sperms, have Wolbachia because the bacteria are shed during spermatogenesis, so CI is mediated by eggs or rather by the Wohbachia they harbor.
- The CI is also very species-specific as in specific for the Wolbachia species.
- Incompatible Wolbachia strains mediating CI has been observed in nature (16).
- Drosophila paulistorum provides evidence for this.
- It has many semispecies that occupy different, slightly overlapping geographic areas (17).
- These semispecies show strong sexual isolation which correlated with each harboring a different Wolbachia species.
- When semispecies are crossed, <10% of embryos survive, and all males are sterile (18).
- When these semispecies were antibiotic Rx, i.e., ‘cured’ of Wolbachia, their sexual isolation immediately decreased (18).
- Scientists also showed Wolbachia‘s role in sexual selection/isolation in lab-maintained D. melanogaster (19).
- Two separate strains were selected using diet (heavy metals versus ethanol).
- After 30 years, these strains were sexually isolated and differed in their Wohbachia infection status.
- When Wolbachia was removed by antibiotic Rx, sexual isolation between these two strains reduced by ~50%.
II. In Birds
- Breeding kittiwakes have more similar cloacal microbiota compared to non-breeding pairs.
- When direct cloacal contact between breeding pairs was blocked, their cloacal microbial communities diverged.
- Thus, sexual contact between breeding pairs drove their cloacal microbiota to be similar (see figure below from 20 showing a graphical representation of the data in 21).
- This study indicates horizontal exchange of microbiota during sex.
- Does shared microbiota influence fecundity/reproductive fitness? As yet unknown.
Thus, data from a wide variety of animals shows that microbiota influence mating preference.
- Two general principles also emerge. Symbiotic microbiota
- Can influence host reproduction by providing them essential nutrients lacking in their diets. In other words a selective advantage without which hosts may be unable to develop or reproduce normally.
- Can selectively inhibit matings that decrease chances of their own transmission.
- Evidence in humans? No data yet. However, it’s early days. After all, the field’s still in its infancy.
- Sharon, Gil, et al. “Commensal bacteria play a role in mating preference of Drosophila melanogaster.” Proceedings of the National Academy of Sciences 107.46 (2010): 20051-20056.
- Rosengaus, Rebeca B., et al. “Disruption of the termite gut microbiota and its prolonged consequences for fitness.” Applied and environmental microbiology 77.13 (2011): 4303-4312.
- Ben-Yosef, Michael, et al. “Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion.” Proceedings of the Royal Society of London B: Biological Sciences (2010): rspb20092102.
- Knipling, E. F. “Possibilities of insect control or eradication through the use of sexually sterile males.” Journal of Economic Entomology 48.4 (1955): 459-462.
- Hendrichs, J., et al. “Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behavior studies.” Florida Entomologist 85.1 (2002): 1-13.
- Ami, Eyal Ben, Boaz Yuval, and Edouard Jurkevitch. “Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance.” The ISME journal 4.1 (2010): 28-37.
- Yuval, B., et al. “The Mediterranean fruit fly and its bacteria–potential for improving sterile insect technique operations.” Journal of Applied Entomology 137.s1 (2013): 39-42.
- Gavriel, S., et al. “Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies.” Journal of Applied Entomology 135.7 (2011): 564-573.
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- Augustinos, Antonios A., et al. “Exploitation of the Medfly Gut Microbiota for the Enhancement of Sterile Insect Technique: Use of Enterobacter sp. in Larval Diet-Based Probiotic Applications.” PloS one 10.9 (2015): e0136459.
- Werren, John H., Donald Windsor, and Lirong Guo. “Distribution of Wolbachia among neotropical arthropods.” Proceedings of the Royal Society of London B: Biological Sciences 262.1364 (1995): 197-204.
- Werren, John H. “Biology of wolbachia.” Annual review of entomology 42.1 (1997): 587-609.
- Serbus, Laura R., et al. “The genetics and cell biology of Wolbachia-host interactions.” Annual review of genetics 42 (2008): 683-707.
- Hilgenboecker, Kirsten, et al. “How many species are infected with Wolbachia?–a statistical analysis of current data.” FEMS Microbiology Letters 281.2 (2008): 215-220.
- Ringo, John, Gil Sharon, and Daniel Segal. “Bacteria-induced sexual isolation in Drosophila.” Fly 5.4 (2011): 310-315.
- Bordenstein, Seth R., and John H. Werren. “Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia.” Heredity 99.3 (2007): 278-287.
- Dobzhansky, Th, Lee Ehrman, and P. A. Kastritsis. “Ethological isolation between sympatric and allopathic species of the Obscura group of Drosophila.” Animal behaviour 16.1 (1968): 79-87.
- Miller, Wolfgang J., Lee Ehrman, and Daniela Schneider. “Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.” PLoS Pathog 6.12 (2010): e1001214.
- Koukou, Katerina, et al. “Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations.” Evolution 60.1 (2006): 87-96.
- Archie, Elizabeth A., and Jenny Tung. “Social behavior and the microbiome.” Current Opinion in Behavioral Sciences 6 (2015): 28-34.
- White, Joël, et al. “Sexually transmitted bacteria affect female cloacal assemblages in a wild bird.” Ecology letters 13.12 (2010): 1515-1524.