Project 1: Characterizing 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 the mechanisms underlying these forms of reproductive sabotage remain largely a mystery. We will begin characterizing the mechanisms of symbiont-induced reproductive sabotage in spiders using a combination of organismal biology, bioinformatics, and fluorescent microscopy. The main host system is a dwarf sheet-web spider, Mermessus fradeorum, that is found in alfalfa fields across the US. This spider is host to at least 5 different heritable symbionts, including a Rickettsiella strain that causes CI and a Wolbachia strain that feminizes male spiders. Curiously, feminization is improved when Wolbachia co-infects spiders with other symbionts.
We’re interested in learning more about how Rickettsiella and Wolbachia sabotage spider reproduction, including what developmental processes these symbionts disrupt, what symbiont factors are involved in this sabotage, and how co-infection with multiple symbionts alters the sabotage process. Identifying manipulation effectors can provide insight into the evolution of reproductive manipulation across distantly related bacteria.
Project 2: Exploring how environmental variation influences heritable symbioses
Heritable symbionts often respond poorly to environmental variation, leaving them susceptible to even mild changes in their environment. This environmental sensitivity is thought to be a consequence of their host-restricted intracellular lifecycles, which results in largescale genomic decay, and in turn reduces their capacity to respond to stress. Yet in spite of their susceptibility to temperature, heritable symbionts persist in natural host populations that experience variable environments. How do heritable symbionts withstand these fluctuating thermal conditions? In most cases we don’t know, but considering how intertwined these bacteria are with their arthropod hosts, these heritable symbionts likely play roles in mediating arthropod responses to to environmental variation.
Using spiders as models, we will explore how variation in temperature, a common environmental stressor for symbionts, affects symbiosis stability in the lab and the field. We will also begin exploring how temperature influences symbiont gene expression and localization to better understand the genetic underpinnings of symbiont stress responses. We plan on pairing these lab-based studies with surveys of spider populations to observe how vary in symbiont infection frequencies vary 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 (another sheet-weaver), and Glenognatha foxi (long-jawed orbweaver). All three spider species host multiple symbionts that display geographic variation in infection frequency, making them excellent models for studying how the external environment shapes symbiont communities.
Project 3: Characterizing heritable symbioses of spiders
Spiders are a common but often misunderstood and under studied 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 fields across 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.