Maxine Zylberberg

  • Postdoctoral Fellow
  • Ornithology & Mammalogy
  • PhD

Please click here to visit my current website for up-to-date information on my research.

 

Last updated Spring 2013

 

I take a multi-disciplinary approach to the study of disease ecology and pathogen evolution, drawing from the fields of ethology, behavioral ecology, immunology, and metagenomics to inform my study of disease dynamics in wild bird populations. I am particularly interested in how variation in host behavior, immunology, and ecology affect disease dynamics across a variety of geographical and temporal scales, from seasonal disease dynamics, to small and large scale geographic variation in pathogen prevalence, to pathogen evolution.

 

   Aggressive interaction between small ground finches at a feeding station, Galapagos, Ecuador

 

   Assay measuring innate immune function )natural antibodies and complement)               

From top left: aggressive interaction between male small ground finches at a feeder station, Galapagos, Ecuador; immune assay measuring two aspects of immune function (natural antiobodies and complement); viral detection microarray (red spots indicate a viral "hit")

 

Current Research Focus:

Viral biogeography

Birds are known zoonotic sources of human infection that have the ability to rapidly spread disease across large geographic areas. However, relatively little is known about the composition of their pathogen communities, or what factors underlie the diversity of those communities. Using samples from an array of Papua New Guinea avian species across 20 islands, I am using high-throughput metagenomic sequencing to conduct an initial survey of the avian virome (or viral community). I will use this data to explore the factors underlying the observed biogeography of viruses (for example, how do island size, isolation, ecological community, and human disturbance underlie variation in viral communities between islands?). 

 

Breakdown of deep sequencing reads by domain from a cloacal swab sample of a single individual; viruses accounted for just over 10% of sequences present


 

Avian virome diversity

Behavioral and ecological variation are important determining factors in the spread of infectious disease. This suggests that behavioral and ecological variation between species may, in turn, have important ramifications for the composition and diversity of the pathogen communities of those species. The Farallon islands are host to a rich avifauna that varies widely in both behavior and ecology. I am making use of this variation to test hypotheses regarding the drivers of virome  (viral community) diversity across species as related to behavioral variation, variation in species ecology, and variation in life history strategies. I am also working with collaborators to survey the viromes of red-tailed hawks and black capped chickadees.

 

    

From left: a wstern gull, one of the species being surveyed as part of the Farallon Islands project; collecting and processing blood sampels from a red-tailed hawk

 

Ongoing Research:

Disease ecology of avian pox in the Galapagos avifauna

Avian pox virus has been implicated in population extinctions in the Hawaiian avifauna and has been present in the Galapagos for approximately 100 years, yet relatively little remains known about the impact of this pathogen on the iconic Galapagos avifauna. In this context, I take an interdisciplinary approach to studying the dynamics of avian pox virus in the Galapagos finches. Specifically, I combine longitudinal data on disease prevalence and recovery rates with behavioral, immunological, and ecological data to explore how and why the impact of avian pox virus varies between Galapagos finch species.

 

Collecting a sample from a medium ground finch for subsequent immune measurement     Active avian pox lesion

From left: collecting a blood sample from a medium ground finch for later immunological analysis; an active avian pox lesion

 

Population heterogeneities and disease dynamics

Interest in wildlife disease ecology has grown steadily in the past two decades as a result of the recent emergence of infectious diseases of conservation and public health importance. However, population heterogeneities (for example, in behavior or physiology) that can alter exposure and susceptibility to pathogens, thereby determining the course of epidemics, are largely ignored. I am particularly interested in understanding the factors that underlie individual and group level risk of exposure to and susceptibility to pathogens and the relationship between those underlying factors. To this end, I study 1) behavioral disease defenses (house finches and Galapagos finches), 2) the physiological and ecological factors that contribute to seasonal pathogen emergence and individual variation in pathogen load (red crossbills and mountain white-crowned sparrows), and 3) physiological trade-offs underlying individual variation in immune function (house finches). The last two research areas stem from ongoing collaborations.

 

Mountain white-crowned sparrow, Tioha Pass, CA     House Finch     Haemoproteus parasite in teh red blood cell of a red crossbill

From left: a mountain white-crowned sparrow, Tioga pass, CA; a house finch; haemoproteus parasites infecting the red blood cells of a red crossbill

Please click here to visit my current website for an up-to-date copy of my CV.

 

Last updated Fall 2013

 

Maxine Zylberberg

Postdoctoral Research Fellow

University of California, San Francisco

Byers Hall, 1700 4th St., Room 403, San Francisco, CA, 94158

MaxineZylberberg at gmail dot com

 

Education

Ph.D., Animal Behavior, University of California, Davis, 2011.

with a degree certificate in Conservation Management.

B.A., Biology, Amherst College, 2001. Magna cum Laude, departmental honors. 

 

Positions Held

NSF Postdoctoral Research Fellow, University of California, San Francisco, 2013(-2016)

Postdoctoral Research Fellow, California Academy of Sciences, 2011-2013

Postdoctoral Research Associate, University of California, San Francisco, 2012-2013

 

Research Highlights

Postdoctoral Research, Department of Ornithology and Mammalogy, California Academy of Sciences.

Diversity and distribution of viral communities in the Papua New Guinea avifauna

Ecological correlates of viral diversity in colonially nesting seabirds

Underlying causes of avian keratin disorder in black capped chickadees

Doctoral Research, Neurobiology, Physiology, and Behavior, University of California, Davis.

Disease ecology, behavior, and immunology of avian pox in Galápagos finches

Immunology and behavior of house finches

Ongoing Collaborative Projects

Affect of plasmodium and haemoproteus infection on mountain white-crowned sparrow fitness

Physiological determinants of seasonal variation in red crossbill haematozoan infections

Research Associate, Biochemistry and Biophysics Department, UCSF 2001-2002.

Developed microarray for viral detection, identifying causative agents of diseases of unknown etiology

Undergraduate Honors Thesis Research, Biology Department, Amherst College, 2000-2001.

Evolution of virulence in Bangladeshi cholera strains isolated from 1971 to 2001 

 

Fellowships, Grants, and Awards (selected)

Allen G. Marr Distinguished Dissertation Award in Biological Sciences for 2011-2013, UC Davis, 2013.

National Science Foundation Postdoctoral Research Fellowship, 2012; $250,500.

National Science Foundation Graduate Research Fellowship, 2006; $120,000.

Summer Institute in Statistics and Modeling of Infectious Disease Scholarship, 2012; $1,950.

University of California, Davis, Office of Graduate Studies Fellowship, 2009; $32,500.

Animal Behavior Graduate Group mini-fellowship, 2009; $400.

American Ornithologists’ Union Research Grant, 2008; $1700.

Hemispheric Institute on the Americas Summer Research Grant, 2008; $1500.

Sigma Xi Grant-in-Aid of Research, 2008; $1000.

University of California, Davis, Office of Graduate Studies NSF Research Grant, 2007; $3000.

Ford Diversity Fellowship, 2006 (declined); $90,000.

Stockton Sportsman's Club Research Grant, 2006; $250.

University of California, Davis, Dean's Fellowship, 2005; $16,000.

Animal Behavior Graduate Group Block Grant, 2004; $8,000.

 

Publications

1.Zylberberg, M., Klasing, K., Hahn, T. P. Exploratory behavior, not plumage color, predicts immune function in house finches (Carpodacus mexicanus). In review.

2. Zylberberg, M., Derryberry, E. P., Breuner, C. W., Macdougall-Shackleton, E. A., Cornelius, J. M., Hahn, T. P. Impacts of avian malaria and related parasites on lifetime reproductive success and survivorship in a migratory songbird. In review.

3. Zylberberg, M. Optimizing disease defense strategies: Galápagos finches balance investment in behavioral and immune defenses. In review.

4. Cornelius, J., Zylberberg, M., Breuner, C., Hahn, T. P. Assessing the role of reproduction and stress in the spring emergence of Haematozoan parasites in birds. Accepted. The Journal of Experimental Biology.

5.Zylberberg, M., Klasing, K., Hahn, T. P. House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defenses against pathogens. In press. Biology Letters.

**Press Coverage: The Raw Story; Channel News Asia; Agence France-Presse; Science Today, California Academy of Sciences

6.Zylberberg, M., Lee, K., Klasing, K., Wikelski, M. Change in avian pox prevalence varies by species and land use type in Galápagos finches. In press. Conservation Biology.

**Press Coverage: SICB Science News, Society for Integrative and Comparative Biology

7.Schwartz, M,. Deiner, K., Forrester, T., Grof-Tisza, P., Muir, M., Santos, M., Souza, L., Wilkerson, M., Zylberberg, M. Perspectives on the Open Standards for the Practice of Conservation. Biological Conservation, 155, 169-177.

8.Zylberberg, M., Lee, K., Klasing, K., Wikelski, M. Behavior and immune function, but not infection status, vary with plumage color in Galápagos finches. 2012. Biological Conservation, 153, 72-79.

**Press Coverage: SICB Science News, Society for Integrative and Comparative Biology

9.Elbroch, L., Mwampamba, T., Santos, M., Zylberberg, M., Liebenberg, L., Minye, J., Mosser, C., Reddy, E. The value, limitations and challenges of employing local experts in conservation research. 2011. Conservation Biology, 25, 1195-1202.

10.  Wang, D., Coscoy, L., Zylberberg, M., Avila, P.C., Boushey, H.A., Ganem, D., DeRisi, J.L. 2002. Microarray-based detection and genotyping of viral pathogens. Proc Natl Acad Sci, 99, 15687-15692.

 

Abstracts and Presentations

1. Zylberberg, Klasing, K.C., Hahn, T.P. House finches (Carpodacus mexicanus) balance investment in behavioral and immunological defenses against pathogens. Annual Meeting of the Society for Integrative and Comparative Biology (SICB), 2013.

2. Zylberberg, M., Lee, K.A., Klasing, K.C., Hahn, T.P., Wikelski, M. Change in Avian Pox prevalence varies by species and land use type in Galapagos finches. SICB, 2012.

3. DeCastro, D.M., Zylberberg, M., Brazeal, K.R., Hahn, T.P. Effects of various photoperiod treatments on the molt schedule of house finches. SICB, 2012.

4. Zylberberg, M., Klasing, K. C., Hahn, T.P. House finch social behavior varies with immune function and partner health to reduce infection risk. Animal Behavior Society, 2011.

5. Cornelius, J.M., Zylberberg, M., Breuner, C.W., Hahn, T.P. Reproductive status and hematozoan parasite load in the opportunistically breeding and nomadic red crossbill, Loxia curvirostra. SICB, 2007.

6. Zylberberg, M., Cornelius, J.M., Breuner, C.W., Hahn, T.P. Reproductive status and haemosporidian parasite load in the Red Crossbill, Loxia curvirostra. ABGG Biennial Conference, 2007.

 

Teaching Experience

Teaching Assistant, Introductory Biology (Evolution), Dept. of Evolution and Ecology, UC Davis, 2007.

Guest Lecturer, Animal Behavior Graduate Student First Year Seminar, 2006.

Teaching Assistant, Introductory Biology (Evolution), Dept. of Evolution and Ecology, UC Davis, 2005.

Guest Lecturer, Animal Behavior Graduate Student First Year Seminar, 2005.

Teaching Assistant, Introductory Geology, Amherst College, 1999.

 

Academic Service

Postdoctoral Representative to the Animal Behavior Committee of SICB, 2012(-2014).

Manuscript Reviewer, Journal of Wildlife Diseases, Auk, ongoing.

Executive Committee, Animal Behavior Graduate Group, UC Davis, 2008-2010.

Advising Committee, Animal Behavior Graduate Group, UC Davis, 2006-2009.

Graduate Student Adviser, Animal Behavior Graduate Group, UC Davis, 2006-2009.

Co-organizer of departmental seminar series, Animal Behavior Graduate Group, UC Davis, 2006-2008.

Representative to the Graduate Student Association, UC Davis, 2006-2007.

Organizer and Facilitator of the Animal Behavior Graduate Student Weekly Meeting, 2005-2007.

Coordinator of the Graduate Student First Year Seminar, Animal Behavior Graduate Group, 2005-2006.

 

Community Science Education

Environmental Educator, UC Davis Arboretum Naturalist Program, 2008.

WIDSI Science Teacher, 2004-2007. Through bi-weekly classes, this small campus group aims to improve science education for "at risk" youth the area.

Society for Conservation Biology, UC Davis Chapter Educational Outreach Group Leader, 2005. Co-planned and lead a biology based exchange program between public elementary school kids in Davis, CA, and La Paz, Bolivia.

A Better Chance House Math and Science Tutor for “at risk” youth, 1998-2001.

 

Professional Affiliations 

Society for Integrative and Comparative Biology (Committee Member, Division of Animal Behavior)

American Ornithologists’ Union

Sigma Xi Honorary Research Society

Society for Conservation Biology

Animal Behavior Society

Please click here to visit my current website for up-to-date information on publications.

 

Last updated Fall 2013

 

1. Zylberberg, M., Klasing, K., Hahn, T. P. In house finches (Carpodacus mexicanus), risk takers invest more in innate immune function. In review.

Overview: Consistent individual behavioral differences can lead to variation in exposure to pathogens. In particular, exploratory individuals appear more likely to be exposed to novel pathogens than less-exploratory individuals. Here, we test the hypothesis that immune function is inversely related to behaviors with the potential to decrease exposure to pathogens (i.e., forgoing exploratory behaviors). We show that individuals that engage in low-risk behaviors in a novel situation invest less in innate immune function than individuals engaging in high-risk behaviors. This individual variation in pathogen defense strategies is expected to affect the dynamics of pathogen spread through populations, and ultimately the course of epidemics. The incorporation of variation in disease defense strategies into models of wildlife disease dynamics we will improve our ability to understand, model, and predict the outcomes of pathogen spread in wildlife.

 

2. Zylberberg, M., Derryberry, E. P., Breuner, C. W., Macdougall-Shackleton, E. A., Cornelius, J. M., Hahn, T. P. Impacts of avian malaria and related parasites on lifetime reproductive success and survivorship in a migratory songbird. In review.

Overview: The impact of haematozoan infection on host fitness has received substantial attention since Hamilton and Zuk posited that parasites are important drivers of sexual selection. Interactions between haematozoan parasites and their avian hosts are frequently used to model fundamental questions in ecology and evolution; however, the assumption that these parasites consistently reduce host fitness in the wild has yet to be conclusively established. To this end, we conducted a long-term study examining the relationship between naturally-occurring infection with Haemoproteus and Plasmodium, and lifetime reproductive success and survival of mountain white-crowned sparrows (Zonotrichia leucophrys oriantha). Specifically, we tested the hypothesis that birds infected with haematozoan parasites should have reduced survival (as determined by overwinter return rates) and reproductive success. Contrary to expectation, we found that Haemoproteus-infected females exhibited a trend towards increased annual reproductive success and had significantly higher overwinter return rates, with the result that these females fledged more than twice as many chicks during their lifetimes as did uninfected females. We discuss the impact of parasitic infections on host fitness in light of these findings and suggest that, in the case of less virulent pathogens, investment in excessive immune defense may decrease lifetime reproduction.

 

3. Zylberberg, M. Optimizing disease defense strategies: Galápagos finches balance investment in behavioral and immune defenses. In review.

Overview: The importance of behavior in disease spread in wildlife has long been recognized by the scientific community, and recent studies have highlighted the potential for behavior to act as a disease defense strategy. This suggests that organisms may benefit from balancing investment in immunological and behavioral pathogen defenses as both are costly but serve a common function. I hypothesize a broad relationship between individual behavior and immune function and test this hypothesis using data from observations of wild Galápagos finches at feeders combined with field collected immune data. I show that, both within and between species, those groups engaging in more high transmission-risk behaviors (not investing in behavioral defenses against disease) invest more heavily in immune disease defenses. I conclude that the relationship between behavior and immune function is more complex than previously thought and demands further attention to understand the ramifications of individual immunological and behavioral variation for disease ecology in wildlife.

 

4. Cornelius, J., Zylberberg, M., Breuner, C., Hahn, T. P. Assessing the role of reproduction and stress in the spring emergence of Haematozoan parasites in birds. Accepted. The Journal of Experimental Biology.

Overview: Many birds experience a relapse in parasite infection during breeding, but the factors underlying this “spring peak” remain poorly understood. We evaluated the relationship between hematozoan parasite load and potential predictors such as month, breeding condition, sex, molt, body condition and corticosterone levels in the nomadic and opportunistically breeding red crossbill, Loxia curvirostra. Opportunistic species breed on schedules that differ from most birds and therefore offer a unique opportunity to investigate the relationship between reproductive condition, season, and parasite load. We do not find evidence that physiological stress associated with reproduction is the cause of the ubiquitous spring peak in blood parasite load. Instead, both seasonal vector activity and relapse of latent infections remain potential underlying factors in the observed spring peak.

 

5. Zylberberg, M., Lee, K., Klasing, K., Wikelski, M. Variation with land use of immune function and prevalence of avian pox in Galápagos finches. 2013. Conservation Biology, 27,103-112

Overview: Infectious disease has been implicated in recent wildlife extinctions and population declines world wide. Both anthropogenic-induced change and natural environmental features can impact pathogen spread. Meanwhile, environmental disturbance can result in changes in stress physiology, nutrition, and social structure, which in turn can suppress immune system function. It remains unknown whether landscape variation results in variation in host resistance to pathogens in general, and in immune function in particular. Avian pox virus, implicated in avian declines and extinctions in Hawaii, was introduced to the Galápagos in the 1890’s, and prevalence has recently increased in Galápagos finches. We test two hypotheses regarding geographic and temporal variation in pox prevalence in seven species of finch: specifically, that prevalence and recovery trends in finches vary by elevation or human land use. In addition, we determined whether annual changes in four aspects of innate immune function (complement, natural antibodies, PIT54 protein, and heterophil:lymphocyte ratio) vary by elevation or land use. We found no variation in prevalence and recovery rates by elevation from 2008 to 2009. In agricultural areas, there was a more than eight-fold increase in avian pox prevalence (from 2% to 17%), while there was no change in prevalence in urban or undeveloped areas. Furthermore, we show that variation in immune function across human land use types correlates with variation in both increased prevalence and susceptibility, indicating that changes in innate immune function may underlie changes in disease susceptibility. Our results suggest that human disturbance, in particular agricultural practices, could underlie immunological changes in host species which contribute to pathogen emergence.

 

**Press Coverage: SICB Science News, Society for Integrative and Comparative Biology

 

6. Zylberberg, M., Klasing, K., Hahn, T. P. House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defenses against pathogens. 2012. Biology Letters (doi: 10.1098/rsbl.2012.0856).

Overview: Infection with pathogens is costly for hosts. In response, animals have evolved behavioral and immunological strategies to avoid pathogen infection. Scientists usually study these strategies in isolation; however, since these defenses are themselves costly, host individuals should benefit from balancing investment in them, and understanding of disease dynamics would benefit from studying the relationship between them. We show that house finches avoid sick individuals, and that individuals who invest less in behavioral defenses invest more in immune defenses. This variation has important implications for the dynamics of pathogen spread through populations, and the course of epidemics overall.

 

**Press Coverage: The Raw Story; Channel News Asia; Agence France-Presse; Science Today, California Academy of Sciences

 

7. Schwartz, M,. Deiner, K., Forrester, T., Grof-Tisza, P., Muir, M., Santos, M., Souza, L., Wilkerson, M., Zylberberg, M. Perspectives on the Open Standards for the Practice of Conservation. 2012. Biological Conservation, 155, 169-177.

Overview: The Open Standards for the Practice of Conservation (OS), and its software platform Miradi, are becoming central tools for conservation management. We applied the OS, using Miradi, to five widely varied conservation projects as the foundation for this perspective. We find, in general, that the OS are logical, clear, and provide a robust hierarchical structure from which to organize management action and track progress toward conservation project goals. One goal of the Conservation Measures Partnership in creating the OS is to foster a community of practice for conservation. We develop and discuss a series of recommendations too better accomplish this goal and call on both academics and the conservation practitioners to better engage with one another for the benefit of training, cross-project learning and better conservation action.

 

8. Zylberberg, M., Lee, K., Klasing, K., Wikelski, M. Increasing avian pox prevalence varies by species, and with immune function, in Galápagos finches. 2012. Biological Conservation, 153, 72-79.

Overview: Avian pox virus (APV), a pathogen implicated in avian declines and extinctions in Hawaii, was introduced to the Galápagos in the late 1890s. While APV is thought to have increased in prevalence in recent years, no study has carefully evaluated the threat this pathogen poses to the Galápagos avifauna. We examine the course of the APV epidemic in seven species of Galápagos finch on Santa Cruz Island. We describe temporal changes in the prevalence of the avian pox disease (AP) caused by APV and the proportion of individuals that have recovered from AP from 2000 to 2009. Then we examine species differences in susceptibility to AP and how this variation correlates with differences in innate immune function. We show that AP prevalence has increased dramatically in the past decade. However, this increase in prevalence varied by species, with prevalence increasing rapidly in G. fuliginosa, C. parvulus, G. scandens, and C. olivacea, but not at all in G. fortis. Furthermore, innate immune function varies between years and species, and this variation correlates with increased prevalence and species variation in susceptibility to APV. This is the first study, to our knowledge, to demonstrate significant interannual variation in innate immune function in wild birds, and to show that this immune variation correlates with susceptibility to an introduced disease.

 

**Press Coverage: SICB Science News, Society for Integrative and Comparative Biology

 

9. Elbroch, L., Mwampamba, T., Santos, M., Zylberberg, M., Liebenberg, L., Minye, J., Mosser, C., Reddy, E. The value, limitations and challenges of employing local experts in conservation research. 2011. Conservation Biology, 25, 1195-1202.

Overview: Evidence suggests that the involvement of local people in conservation work increases a project’s chances of success. However, involving citizen scientists in research, raises questions about data quality. To better assess potential participants for conservation projects, we developed a knowledge gradient, K, along which community members occupy different positions on the basis of their experience with and knowledge of a research subject. This gradient can be used to refine the citizen–science concept and allow researchers to differentiate between community members with expert knowledge and those with little knowledge. We propose that work would benefit from the inclusion of select local experts because it would allow researchers to harness the benefits of local involvement while maintaining or improving data quality. We used a case study from the DeHoop Nature Preserve (South Africa) in which we evaluated the expert’s knowledge and analyzed the data he collected. The data collected by J.J. are consistent with the notion that involving local experts can produce reliable data. Finally, we developed a conceptual model to help identify the appropriate participants for a given project on the basis of research budget, knowledge or skills needed, technical literacy requirements, and scope of the project.

 

10.  Wang, D., Coscoy, L., Zylberberg, M., Avila, P.C., Boushey, H.A., Ganem, D., DeRisi, J.L. 2002. Microarray-based detection and genotyping of viral pathogens. Proc Natl Acad Sci, 99, 15687-15692.

Overview: The detection of viral pathogens is of critical importance in biology, medicine, and agriculture. Unfortunately, existing techniques to screen for a broad spectrum of viruses suffer from severe limitations. To facilitate the comprehensive and unbiased analysis of viral prevalence in a given biological setting, we have developed a genomic strategy for highly parallel viral screening. The cornerstone of this approach is a long oligonucleotide (70-mer) DNA microarray capable of simultaneously detecting hundreds of viruses. Using virally infected cell cultures, we were able to efficiently detect and identify many diverse viruses. Related viral serotypes could be distinguished by the unique pattern of hybridization generated by each virus. Furthermore, by selecting microarray elements derived from highly conserved regions within viral families, individual viruses that were not explicitly represented on the microarray were still detected, raising the possibility that this approach could be used for virus discovery. Finally, by using a random PCR amplification strategy in conjunction with the microarray, we were able to detect multiple viruses in human respiratory specimens without the use of sequence-specific or degenerate primers. This method is versatile and greatly expands the spectrum of detectable viruses in a single assay while simultaneously providing the capability to discriminate among viral subtypes.