Arthropod-Microbe Symbioses

Most multicellular organisms engage in some sort of symbiosis with their microbial neighbors. These symbioses are especially common and diverse in terrestrial arthropods. My research focuses on heritable symbioses between arthropods and maternally transmitted endosymbiotic bacteria. These bacteria are often intracellular, infect a range of host tissues, and can have substantial effects on their host’s biology. These effects include supplementing host nutrition, protecting the host against important natural enemies, and manipulating host reproduction to favor females that spread the bacteria. I am particularly interested in bacterial symbionts that manipulate host reproduction, which can influence arthropod evolution and speciation. These reproductive manipulators also have potential applications in the control of arthropod populations and the spread of insect-vectored diseases like Dengue.

My research focuses on exploring the internal and external interactions that shape these symbioses. Inside the host, this involves characterizing the cellular and molecular processes that lead to novel symbiont-induced phenotypes and exploring how elements of the host environment, like other coinfecting intracellular bacteria, alter these processes. Outside the host, I’m interested in understanding how climatic factors like temperature alter host-bacteria dynamics.

Read on for more info on our current research projects

Project 1: Characterization of the cellular and molecular mechanisms of reproductive manipulation

Some of the most successful host-associated bacteria on earth are heritable symbionts that manipulate host reproduction. Some of these bacteria turn males (dead-end hosts) into females (feminization), others cause infected females to asexually produce more infected females (parthenogenesis). The most common form of manipulation is cytoplasmic incompatibility (CI); sabotage that benefits infected females by weaponizing male hosts to kill uninfected offspring. These reproductive saboteurs are diverse and common, but we still don’t know much about how they cause these different effects in their hosts. We will begin characterizing the mechanisms of symbiont-induced reproductive sabotage using a combination of organismal biology, bioinformatics, and fluorescent microscopy. This project includes two symbiosis systems. The first is a dwarf sheet-web spider, Mermessus fradeorum (linyphiidae), that is found in alfalfa fields across the US. This spider is host to at least 5 different heritable symbionts, including a Rickettsiella that causes CI. This is the first instance of confirmed Rickettsiella-CI, making M. fradeorum a great system to study how this symbiont causes CI. Curiously, when a spider has all 5 symbionts it doesn’t cause CI, instead it is feminized so male hosts develop as females instead. We’re currently trying to figure out which of the 5 symbionts contribute to feminization. The second system we’ll be working on are Encarsia wasps, which are parasitoids of whiteflies that have been used to successfully control populations of the ash whitefly in the US. We have lab cultures of four Encarsia species, each of which are infected with the symbiont Cardinium. Cardinium causes CI in two of the Encarsia species, E. suzannae and E. partenopea, and induces, or is associated with, parthenogenesis in the other two species, E. hispida and E. tabacivora. Our research will continue the work I did for my PhD, which identified the timing of CI induction in male hosts and the localization of Cardinium within host gonads during the CI induction window.

Female Mermessus fradeorum

Left image: A pupal male E. suzannae removed from its whitefly host. Right image: Confocal fluorescent image showing a testis of pupal E. suzannae. Cardinium cells are colored green, host nuclei are blue. Cardinium can be seen infecting developing sperm cells (circular nuclei) but trails elongating nuclei. No Cardinium are seen in the seminal vesicle housing mature sperm (orb with long hair-like nuclei at base of image). Images from Doremus et al. 2020 Frontiers in Microbiol.

Project 2: Effects of climate on heritable symbioses

Male Glenognatha foxi, displaying his prodigious pedipalps. Male spiders use their pedipalps during copulation.

Heritable symbionts are notoriously bad at handling environmental stress, particularly thermal stress. Their host-restricted intracellular lifecycles lead to largescale genomic decay, which in turn reduces their capacity to respond to stress. This is problematic considering our planet is undergoing a global climatic shift, bringing with it increasing and more variable temperatures. How will climate change affect these widespread symbioses? Currently we don’t know, but considering how intertwined these bacteria are with their arthropod hosts, these heritable symbionts will likely play a big part in how arthropods themselves respond to climate change. Using spiders as models, we will explore how temperature stress affects symbiosis stability in the lab and the field, how temperature influences symbiont gene expression and localization, and how natural populations vary in symbiont infections over geographic and seasonal scales. We have lab cultures of three spider species that vary in their symbiont communities: Mermessus fradeorum (see above), Grammonota inornata (linyphiidae), and Glenognatha foxi (tetragnathidae). All three spider species host multiple symbionts and display some level of geographic variation in infection frequency, making them excellent models for studying how the external environment shapes symbiont communities.

Project 3: Characterization heritable symbioses of spiders

Spiders are a common but often misunderstood arthropod lineage. They provide useful ecological services by suppressing pest populations and many species exhibit complex hunting behaviors and web utilization. They also are often host to complex communities of heritable symbionts, with some species harboring 5 or more symbionts in a single population. These communities are dominated by symbiont species known to manipulate reproduction in other arthropods, like Wolbachia, Cardinium, Rickettsia, and Spiroplasma - but their phenotypic effects are largely uncharacterized in spiders. Why are these symbionts so common in spiders? Before we can answer that question, we need to know more about what the symbionts are doing in spiders. We have begun lab cultures of several spider species commonly found in alfalfa in the US. Each of these species has a different repertoire of symbionts, many of which are implicated in manipulating arthropod reproduction in other hosts. We suspect that at least some of them manipulate their spider host as well. What they do to their host and how they do it remains to be seen.

Top: Female G. foxi munching on a springtail.; Bottom: Female Grammonota inornata ready to lay an egg mass.