A study led by former Duffy Lab postdoc Laura Lopez in 2019 has just appeared in Ecology! The study set out to test for healthy herds predation — where predators can actually increase prey populations as a result of decreasing parasitism. The general idea that predation can benefit prey populations by reducing disease is really pervasive — Meghan’s favorite example comes from this wrapper from a chocolate bar that she bought back when she was a grad student:
This idea that predators can help their prey populations was formalized in a paper in 2003, leading to what has become known as the “healthy herds hypothesis”. As this UMich press release states:
Nature documentaries will tell you that lions, cheetahs, wolves and other top predators target the weakest or slowest animals and that this culling benefits prey herds, whether it’s antelope in Africa or elk in Wyoming.
This idea has been widely accepted by biologists for many years and was formalized in 2003 as the healthy herds hypothesis. It proposes that predators can help prey populations by picking off the sick and injured and leaving healthy, strong animals to reproduce.
The healthy herds hypothesis has even been used to suggest that manipulating predator numbers to protect prey might be a useful conservation strategy. Even so, hard evidence supporting the hypothesis is scarce, and in recent years many of its assumptions and predictions have been questioned.
To test this, Laura led an experiment that manipulated the abundance of phantom midge larvae (which are important predators of zooplankton) and the presence and absence of a fungal parasite in populations of Daphnia dentifera. We found that high predation levels reduced parasitism in Daphnia, providing support for the first half of the healthy herds prediction. However, population sizes of Daphnia were often dramatically reduced.
In addition to Laura and Meghan, the authors are former Duffy Lab undergrad Bruce O’Brien, Mike Cortez of Florida State, Turner DeBlieux and Spencer Hall of Indiana University, and Ilona Menel and Carla Cáceres of U. Illinois.
Kristel has a new paper out in Freshwater Biology asking how toxins produced by cyanobacteria and time spent in the water column influence the infectivity of spores of the common fungal parasite Metschnikowia. This study was inspired by Kristel’s earlier work, published in Proceedings B, which showed that Anabaena and Microcystis diets protected Daphnia against fungal infections. Anabaena and Microcystis are known to produce potent toxins, and Kristel wondered if the protection against infection was due to a direct effect of the toxins on the spores. To test this, Kristel incubated spores in water containing varying levels of toxins for varying amounts of time. She found that toxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, spending longer as a transmission spore decreased a spore’s chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts. These results show both that spores have a limited time to find a new host, and that the protective effect of Anabaena and Microcystis diets on infection is not due to a direct effect of toxins on spores. Here’s a link to the new paper, and here’s the link to the data and code. Baili Zhong and Jorge Agudelo, both of whom were undergraduates in the lab via the Doris Duke Conservation Scholars Program, are coauthors on the study.
Anabaena collected from North Lake near Ann Arbor.
Former postdoc Syuan-Jyun Sun has been writing up projects from his time in the lab, and had four papers come out recently!
First, Sun led an experiment that looked at how temperature modifies trait-mediated infection outcomes in the Daphnia-fungal parasite system that we focus on. This paper was recently published in the ‘Infectious disease ecology and evolution in a changing world’ theme issue of Philosophical Transactions, B that was compiled and edited by Kayla King, Matt Hall, and Justyna Wolinska. In this study, we found that Daphnia reared at warmer temperatures had more robust physical barriers to infection but decreased cellular immune responses during the initial infection process. Infected hosts at warmer temperatures also suffered greater reductions in fecundity and lifespan. Perhaps most interestingly, the relationship between a key trait—gut epithelium thickness, a physical barrier—and the likelihood of terminal infection reversed at warmer temperatures. These results highlight the complex ways that temperatures can modulate host–parasite interactions and show that different defense components can have qualitatively different responses to warmer temperatures. Postdoc Marcin Dziuba and undergrad Riley Jaye are coauthors on this study. The paper can be found here and the data and code from the study can be found here.
Sun followed up with two related studies, one looking at transgenerational effects on parasite fitness, the other looking at transgenerational impacts on host fitness. The study on the impact of transgenerational plasticity on parasite fitness was published in Parasitology (link to paper, link to data & code). In this experiment, we once again exposed Daphnia dentifera to its naturally co-occurring fungal parasite Metschnikowia bicuspidata, rearing the parasite at cooler (20°C) or warmer (24°C) temperatures and then, factorially, using those spores to infect at 20 and 24°C. We found that infections by parasites reared at warmer past temperatures produced more mature spores, but only when the current infections were at cooler temperatures. Moreover, the percentage of mature spores was impacted by both rearing and current temperatures, and was highest for infections with spores reared in a warmer environment that infected hosts in a cooler environment. In contrast, virulence was influenced only by current temperatures. These results highlight the potential for plasticity in parasite traits — something that we think is fascinating and wish more folks worked on! Postdocs Marcin Dziuba and Kris McIntire and undergrad Riley Jaye are coauthors on this paper.
Graphical abstract fromSun et al. Parasitology.
The follow up experiment that focused on transgenerational effects on host fitness recently appeared in Ecology and Evolution (link to paper, link to data & code). In this study, we tested the effects of biotic and abiotic environmental changes on within- and transgenerational plasticity in the Daphnia–Metschnikowia system. By exposing parents and their offspring consecutively to the single and combined effects of elevated temperature and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offsprings of mothers who were exposed to one of the stressors were better able to tolerate elevated temperature, compared with the offspring of mothers who were exposed to neither or both stressors. Yet, the negative effects caused by parasite infection were much stronger, and this greater reduction in host fitness was not mitigated by transgenerational plasticity. We also showed that elevated temperature led to a lower average immune response, and that the relationship between immune response and lifetime fecundity reversed under elevated temperature: the daughters of exposed mothers showed decreased fecundity with increased hemocyte production at ambient temperature but the opposite relationship at elevated temperature. Postdoc Marcin Dziuba and undergrad Riley Jaye are coauthors on this study.
Finally, Sun has a paper in press at Functional Ecology that explores the ways in which host and parasite functional morphology influence the outcomes of host-parasite interactions. This work uses the Metschnikowia system again, but in this case isolated Metsch from both Daphnia dentifera and Ceriodaphnia dubia, building on earlier work by Clara Shaw. We studied how host gut traits, parasite spore size and host immune responses influenced the infection process. We collected parasite spores from two host species, the larger Daphnia dentifera and the smaller Ceriodaphnia dubia, and exposed both host species to spores sourced from each host. The ability of a spore to embed in the host gut and to penetrate into the body cavity was influenced by the host species that was exposed to the parasite (‘exposure host species’) and the species from which the spores were sourced (‘source host species’). Spores sourced from D. dentifera were better able to attack both hosts, but were especially good at attacking D. dentifera. These differences likely resulted from morphological differences, with a striking correspondence between the diameter of host guts and the size of the parasite spores. Immune responses were also influenced by both exposure and source host. Interestingly, only 13.5% of hosts that had at least one parasite spore penetrate ended up with terminal infections; all but one of these infections occurred in D. dentifera hosts exposed to D. dentifera-sourced spores. Lab technician Siobhan Calhoun is a coauthor on this study; the paper can be found here and the data and code can be found here.
Photo (by Syuan-Jyun Sun): The much larger Daphnia dentifera and smaller Ceriodaphnia dubia. Fungal spores isolated from each host are strikingly similar in length to the width of the gut of the species from which they were isolated.
Kate officially became Dr. McLean at the Winter Commencement on December 18th! Congrats again, Kate! Kate has begun a postdoc with Prof. Marisa Eisenberg in Epidemiology at UMich — we’re looking forward to their new work!
Congratulations to Kate, who is now Dr. McLean! Kate’s dissertation included some chapters on the Daphnia-parasite system, plus a chapter on SARS-CoV-2 in Michigan. Kate defended their dissertation last week and is now in the process of doing final edits. Next up for Kate will be a postdoc studying the effects of global change on infectious disease dynamics. It’s a really exciting position: watch this space for more info after everything is official! And congrats, Kate!
Aniqa and Sun both had their last days in the lab in July — we’re sad about them leaving and also excited about their new adventures!
Aniqa worked as an undergrad researcher in the lab beginning in Fall 2019 (in the before times!), working particularly closely with Kristel. (Fun fact: Aniqa also worked on fixing captions on Intro Bio videos during the 2020-2021 school year!) Aniqa will be starting an MS program in Physiology here at Michigan this fall.
Sun began as a postdoc in the lab in 2021, and to say that he hit the ground running would be an understatement! Sun did lots of fieldwork (and took gorgeous photos of our lakes!) and also carried out a series of lab experiments. Sun is now moving back to Taiwan where he will begin a faculty position at National Taiwan University. Check out his website!
A beautiful sunrise at Whitmore Lake (photo credit: Syuan-Jyun Sun)
One of Kate McLean’s dissertation chapters just appeared in Evolutionary Ecology!The paper explored the roles of sexual recombination and temporal gene flow (via the egg bank) in maintaining host resistance and genetic diversity. Many studies (including some from our lab) have focused on how host resistance changes within a growing season. Others have looked at long term trends in resistance evolution across many years. Kate’s study looks at the neglected middle ground: how the resistance distribution that exists at the end of one growing season changes by the start of the next growing season as a result of sexual recombination and temporal gene flow from the egg bank.
To study this, Kate and colleagues tracked resistance to Metschnikowia and genetic diversity in Daphnia dentifera in two lakes. This involved collecting sexual females in the autumn, getting them to release their resting eggs, and hatching those resting eggs. Comparing the resistance phenotypes of the moms vs. the hatchlings let us uncover the effect of sexual recombination on resistance, and also to estimate the heritability of resistance. In addition, we sampled the populations early the following spring to characterize the populations shortly after they were reestablished from the egg bank. Since the hatchlings told us about what had gone in to the egg bank the prior year, comparing them with the spring population allowed us to determine the effect of temporal gene flow via the egg bank. Resistance was quantified using infection assays, and genetic diversity was quantified using microsatellites; the diversity component of this project was the foundation of the undergraduate Honors Thesis of Haniyeh Zamani, who is a coauthor on the study.
Because we know that resistance and fecundity trade off in the Daphnia dentifera–Metschnikowia system, we expected that populations would evolve toward higher susceptibility (due to its fecundity advantages) unless an epidemic had recently selected for resistance. Moreover, if an epidemic did occur, we expected resistance to increase temporarily but that sexual recombination and temporal gene flow would then shift the population back towards susceptibility. This is not what we found! Instead, susceptibility was the transient state, with recombination and gene flow restoring and/or maintaining high resistance.
For genetic diversity, we expected that fall offspring would show greater genotypic diversity than their parents due to the effects of sexual recombination; this was observed in one lake (Hackberry) but not in the other (Midland), where genotypic diversity of parents was already very high. We also predicted that the egg bank clones would have higher diversity than the fall offspring, since we anticipated hatching of individuals produced across multiple years; again, this was observed in Hackberry but not in Midland.
In short, sexual recombination and temporal gene flow are both important players in determining inter-annual variation in host resistance in this study system, but not always in the ways we predicted!
In addition to lead author Kate McLean, the authors on this paper are former Duffy Lab grad student Camden Gowler, lab postdoc Marcin Dziuba, former lab undergrad Haniyeh Zamani, long term collaborator Spencer Hall, and Meghan.