My research focuses on how neural mechanisms and experience interact to shape the development and evolution of behavior. I am fascinated with the effects of long-term memory on behavioral decisions in an evolutionary context. My approach applies modern techniques in neurobiology (gene manipulation, electrophysiology, genomics, and imaging), particularly songbirds, to identify the neural mechanisms of long-term memory and recognition systems.
Obligate avian brood parasites are birds that lay their eggs in the nests of other species and then rely on those hosts to raise their parasitic offspring. Although this reproductive strategy is often thought of negatively ("lazy birds"), we still do not understand how brood parasites evolved from non-parasitic ancestors and avoid extinction from host resistance. The strategy is rare (<1% of all bird species), reflecting numerous constraints that prohibit the transition from parental to brood parasitic reproduction. Below are examples of my work which aims to understand the mechanisms, ecology, and evolution that guide behavior, with emphasis on the interaction of innate predispositions and learning.
Obligate avian brood parasites are birds that lay their eggs in the nests of other species and then rely on those hosts to raise their parasitic offspring. Although this reproductive strategy is often thought of negatively ("lazy birds"), we still do not understand how brood parasites evolved from non-parasitic ancestors and avoid extinction from host resistance. The strategy is rare (<1% of all bird species), reflecting numerous constraints that prohibit the transition from parental to brood parasitic reproduction. Below are examples of my work which aims to understand the mechanisms, ecology, and evolution that guide behavior, with emphasis on the interaction of innate predispositions and learning.
NeurOGENOMIC mechanisms for species recognition
In many social animals, early exposure to conspecific stimuli is critical for the development of species-specific behavior. For example, young songbirds learn to sing from ‘tutors’ of their own species. Obligate brood parasitic birds, however, are raised by heterospecific hosts in the absence of conspecific stimuli. Having evolved from a non-parasitic ancestor, how do brood parasites recognize their own species?
Studies of non-parasitic songbirds (e.g. zebra finch) have revealed that the primary and secondary auditory forebrain areas are critical in the differential processing of conspecific vs. heterospecific songs (i.e. species recognition). With functional magnetic resonance imaging (fMRI) and immediate early gene expression (IEG), we find that the same auditory brain regions underlie species recognition in adult Pin-tailed Whydahs (Vidua macroura), a brood parasitic songbird that is sister-taxa to non-parasitic estrildid finches, including the model species zebra finch (Taeniopygia guttata). Articles in Neuroscience Letters, Behavioural Brain Research, and Biological Reviews
One solution to this social recognition paradox is that conspecific identification may be mediated through a non-learned vocal cue, acting as a "password". Female cowbirds produce an non-learned 'chatter' call, which may serve as the password for juveniles. Juvenile cowbirds are better at learning songs if they are played just before the chatter call, even if without prior experience with the female chatter call. Hearing the chatter call induces neuroplasticity and development within the auditory forebrain, a region known to control species recognition. These results suggest that parasitic cowbirds selectively recognize the password chatter, allowing juvenile cowbirds to identify which adults to learn from and avoid mis-imprinting upon unrelated host species. Articles in Current Biology and Journal of Experimental Biology
parasite behavior
Juvenile non-parasitic songbirds generally learn much of their songs and species-specific behaviors by imprinting on parents or siblings. Juvenile parasites, however, are raised in the absence of their own kind; yet somehow recognize their own species and learn appropriate songs and behaviors from conspecifics.
How do brood parasites avoid (mis)imprinting on their own species?
To see how juvenile cowbirds behave in the wild, I used an automated radio-telemetry system that recorded the locations of juveniles and their genetic cowbird mothers every 1-2 minutes. Surprisingly, we found juvenile cowbirds leaving their hosts alone at night, which suggests "innate" roosting preferences may help cowbirds to avoid (mis)imprinting on their hosts. Article at Animal Behavior
How do brood parasites choose their hosts?
Many brood parasites lay eggs in the nests of a single host species. Remarkably, the Brown-headed Cowbird has parasitized over 250 species, many of which are unsuitable surrogates like hawks and ducks! Using long-term data (21 years) and experimental parasitism, I found that cowbirds prefer to parasitize hosts that are best at producing cowbird young. Thus, cowbirds observe the outcome of their own egg-laying decisions and learn how to improve for future attempts. Article in Proc. Roy. Soc. B
To see how juvenile cowbirds behave in the wild, I used an automated radio-telemetry system that recorded the locations of juveniles and their genetic cowbird mothers every 1-2 minutes. Surprisingly, we found juvenile cowbirds leaving their hosts alone at night, which suggests "innate" roosting preferences may help cowbirds to avoid (mis)imprinting on their hosts. Article at Animal Behavior
How do brood parasites choose their hosts?
Many brood parasites lay eggs in the nests of a single host species. Remarkably, the Brown-headed Cowbird has parasitized over 250 species, many of which are unsuitable surrogates like hawks and ducks! Using long-term data (21 years) and experimental parasitism, I found that cowbirds prefer to parasitize hosts that are best at producing cowbird young. Thus, cowbirds observe the outcome of their own egg-laying decisions and learn how to improve for future attempts. Article in Proc. Roy. Soc. B
Host-parasite interactions
Although parasites are extant in nearly every taxonomic group, each parasite must overcome similar selective pressures, such as survival when in association with the host, choosing an appropriate host and, sustainably exploiting the host’s resources. I work with Brown-headed Cowbirds (Molothrus ater), an abundant North American generalist brood parasite, and the Prothonotary Warbler (Protonotaria citrea). These hosts will readily nest in recycled milk-cartons, which provides an efficient method to directly observe behaviors and fitness relationships among parasites and their hosts; typically difficult to quantify within host-parasite systems in nature.
How do brood parasites manipulate host behavior?
Many parasites manipulate the behaviors of their hosts, yet understanding the evolutionary pathways leading to adaptive host manipulation remains unclear. Most species evolved behaviors to compensate for losses in fitness. In birds, females that lose some of their clutch will nest again. However, cowbirds exploit this behavior by reducing the number of warbler offspring and inducing warblers to nest again; thereby increasing the opportunities for parasitism. This appears to enable hosts to recoup some fitness lost to parasitism while simultaneously facilitating parasites to enhance their fitness. Article in Behavioral Ecology
How do cowbirds influence host survival?
To understand the demographic impacts of brood parasitism, or any ecological factor, we must first quantify survival. However, this is exceedingly difficult in migratory birds as the potential for dispersal is vast. By marking 6000 warbler nestlings, and exploring nearly all available habitat for returning birds, I developed a novel multistate mark-recapture model and documented the first juvenile survival probability in a Neotropical migratory songbird. Not only was first-year dispersal and survival much less than presumed for a migratory songbird species, it declined throughout the year and when a warbler fledged with a cowbird nestmate. Article in PLoS ONE
Many parasites manipulate the behaviors of their hosts, yet understanding the evolutionary pathways leading to adaptive host manipulation remains unclear. Most species evolved behaviors to compensate for losses in fitness. In birds, females that lose some of their clutch will nest again. However, cowbirds exploit this behavior by reducing the number of warbler offspring and inducing warblers to nest again; thereby increasing the opportunities for parasitism. This appears to enable hosts to recoup some fitness lost to parasitism while simultaneously facilitating parasites to enhance their fitness. Article in Behavioral Ecology
How do cowbirds influence host survival?
To understand the demographic impacts of brood parasitism, or any ecological factor, we must first quantify survival. However, this is exceedingly difficult in migratory birds as the potential for dispersal is vast. By marking 6000 warbler nestlings, and exploring nearly all available habitat for returning birds, I developed a novel multistate mark-recapture model and documented the first juvenile survival probability in a Neotropical migratory songbird. Not only was first-year dispersal and survival much less than presumed for a migratory songbird species, it declined throughout the year and when a warbler fledged with a cowbird nestmate. Article in PLoS ONE