Current Research

NSF-Funded Research

Pathogen transmission in response to urbanization

Resources and habitat often become limited in urban environments. Urban-adapted species, such as sparrows and finches, are often found at private and public feeders. These feeders tend to have multiple individuals present at the same time, meaning this gregarious lifestyle could lead to an increase in disease transfer. By contrast, passerines in naturalized, rural habitats, feed on plant material such as seeds, buds, and fruit, and are less gregarious, suggesting that rural individuals may not be exposed to the same intensity of social disease transfer. My research team uses standard and quantitative PCR combined with microscopy, to characterize the lineages, prevalence, and infection intensity of microscopic (e.g. bacteria) and macroscopic pathogens, such as ectoparasites (e.g., ticks, lice, and mites), and avian Haemosporidians (malaria) within and between urban and rural populations of passerines.

The evolution of the avian immune system in response to urbanization

Urbanization causes severe habitat destruction with buildings creating barriers between populations. In response to citification, urban bird populations can become less connected, and as a result, can lead to a decrease in gene flow. In songbirds, neutral genetic diversity has been shown to be lower in anthropogenically fragmented landscapes in comparison to naturally fragmented environments. Given that birds may be more susceptible to disease and may have a decrease in genetic diversity due to habitat fragmentation, characteristics of immunity should show spatial variation between cities and rural communities.
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Other Research

parasite-host dynamics

Parasite-host dynamics in songbirds encompass a complex interplay between various microscopic and macroscopic parasites, such as bacteria, viruses, mites, fleas, and ticks, and their hosts. These parasites can severely impact songbird health, leading to diseases that weaken the immune system and may result in death. Infected songbirds often exhibit altered behaviors in feeding, mating, and migration, and can experience reduced reproductive success. In response to these parasitic threats, songbirds have evolved a diverse suite of defense mechanisms, such as behavior and immune responses. This evolutionary arms race extends to parasites too, which adapt by developing methods to evade or resist the host's defenses. These interactions have ecological implications by affecting songbird population dynamics and their role in the broader ecosystem. Conservation efforts, crucial for the protection of vulnerable songbird species, often involve strategies like habitat management and control of parasite vectors, along with vigilant monitoring of disease spread. Looking at how the avian immune system responds to pathogens, and how environmental factors affect their response is an overarching theme in many student projects. My lab researches these dynamics mainly in overwintering ground sparrows, but has opportunities to explore this in breeding birds, and in other passerines.

genetic aspects of Parasite-mediated Sexual Selection

Research on sexual selection usually involves measuring sexually selected traits such as plumage and birdsong, and comparing them to reproductive success or a proxy to fitness. The good genes hypothesis posits that sexually selected traits signals genetic quality whereby the choosier sex would gain indirect (genetic) benefits for their offspring. While there is support for the good genes hypothesis, there is a lack of studies comparing quality of functional genes and sexually selected traits. My lab aims to explore honest signals of immune quality in birds by exploring plumage and birdsong quality and immune genes.

Past Research

Junco Project

Shifts in life-history traits such as seasonal migration can generate parasite-mediated population divergence and speciation. Animals that halt their migratory behavior and remain sedentary year-round will encounter only local parasites, potentially intensifying local arms races. In contrast, migratory animals encounter multiple environments with different parasite communities, potentially favoring diverse immune defenses. Populations that differ in migratory behavior, and the diversity of parasites encountered, should differ in allele frequencies and diversity at immune genes such as the major histocompatibility complex (MHC). We will assess evidence for parasite-mediated divergence at MHC in dark-eyed juncos (Junco hyemalis), using two geographically distinct systems. Migratory and sedentary populations diverged approximately 12,000 years ago in Virginia, but just 37 years ago in California: in each system, migratory and sedentary populations are sympatric during the nonbreeding season. We predict that migratory individuals in each system will be more diverse at MHC, due to balancing selection associated with travel through multiple environments. This difference should be most evident in the historically-diverged (Virginia) system. We will characterize haemosporidian parasites encountered by each of the four populations, and class I MHC diversity within individuals and populations. To unravel effects of selection from those of genetic drift, we will compare differentiation at MHC to neutral-locus differentiation (microsatellite or SNPs derived from restriction site-associated DNA sequencing). With human activities increasingly disrupting migratory routes and behavior, examining parasite-mediated divergence in recently versus historically isolated populations allows forecasting future effects on divergence, and ultimately speciation in action.

***Esther Fernandez (MS) completed this project as her MS thesis.

West Nile Virus in American Robins

A recently emerged and quickly evolving pathogen in North America is the West Nile virus (WNV). This arthropod-borne (e.g. mosquitoes) virus infects a wide variety of animals, such as mammals and birds. A susceptible reservoir host for WNV are American robins (Turdus migratorius), which become infected with WNV more than closely related species but have significant individual variation in infection rate. In order to control for environmental effects of infection, Dr. Jen Owen (Michigan State University) and colleagues infected juvenile robins (food-deprived and normally fed treatments) with WNV in the lab and measured viral titers for each bird. As predicted, there was significant individual variation in infection rate within and between treatments, which implies there may be underlying genetic effects that predicts peak viremia. To understand the coevolution between WNV and robins, we will characterize the major histocompatibility complex (MHC) in these robins and test for protective alleles that may explain the individual variation in viremia. Overall, by focusing on a recently introduced virus, we will gain insights into understanding pathogen-host coevolution through characterizing immune genes that confer disease resistance.

***Parmeet Kaur completed this project as her honors thesis

Dr. Slade’s Past Research

Postdoctoral Research

While acoustic and visual cues are still important, chemical cues are coming into the forefront of communication in songbirds. Recent research, particularly from Dr. Danielle Whittaker, has shown that dark-eyed juncos (Junco hyemalis) respond to chemical cues from preen oil secreted by their uropygial gland. This candidate cue is involved in reproductive success in this species and may be mediated by microbial symbionts located in and around this gland. Alongside Dr. Whittaker, I am trying to unravel how host genotype controls the abundance and taxonomic groups of bacteria in the preen gland of this species.

My other research projects involve investigating the role of adaptive genes in host-pathogen interactions, and how these interactions are involved in population divergence, and animal conservation.

Graduate Research

Ph.D. (Supervisor: Beth MacDougall-Shackleton)

Thesis Abstract: In recent years, sexual selection theory has redefined genetic quality to consider not only additive genetic effects on fitness but also non-additive genetic effects, such as heterozygote advantage or disadvantage. In jawed vertebrates, the major histocompatibility complex (MHC) gene family has been shown to exhibit both additive and non-additive genetic effects on fitness. MHC gene products are involved in initiating adaptive immune responses, and MHC genotype determines the range of pathogens to which an individual can respond. Therefore, parasite-mediated selection at MHC may favour locally-adapted, rare, or particular combination of alleles. Because heterozygote advantage at MHC is widespread, sexual selection should favor mechanisms by which individuals assess the MHC genotypes of potential mates, and mate non-randomly. Studies exploring the role of MHC in immunity and sexual selection are widespread amongst mammals and fish, but in birds (especially songbirds) there is relatively scant evidence for MHC-mediated mating and the mechanism by which this might be accomplished remains unknown. First, I assessed differentiation at MHC class I and II that might underlie locally-good gene effects in two populations of song sparrows (Melospiza melodia) previously shown to exhibit higher resistance to sympatric malaria (Plasmodium) strains. I found no population differentiation, suggesting no locally-good gene effects at MHC, but individuals with higher class I diversity were less likely to be infected when experimentally inoculated with Plasmodium. Second, I explored whether song sparrows convey information on MHC class II genotype through chemical (preen oil) or auditory (birdsong) cues. Pairwise similarity at MHC was related to pairwise similarity of preen oil chemical composition, but not to pairwise similarity in song repertoire content. Song repertoire size, a sexually selected trait in this species, was nonlinearly related to MHC diversity, such that males with intermediate MHC diversity sang the most songs. Finally, to investigate MHC-mediated mate choice, I compared MHC similarity of socially mated pairs of free-living song sparrows to random expectations. Contrary to my prediction of MHC-disassortative mating, social pairs were more similar at MHC than expected by chance. This work emphasizes the importance of considering mate choice in the context of fitness effects at MHC.