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Research

1. Current lines of research

1.1 Urban evolution: evolutionary patterns across species and cities

A main focus of the lab is to investigate how mammals respond to urban environments, especially the impacts of urbanization on reproductive physiology, behavior, and communication across different urban species. My main goal is to explain why some phenotypic traits in a given species always evolve in the same manner across different cities and why the evolution of other traits is city-specific.

Implementing a comprehensive research program across species and cities is a ground-breaking approach for studying ecological and evolutionary dynamics in human-dominated landscapes. Using a comparative framework is critical, because different species may have undergone different processes of adaptation to urban environments, given their different ecological requirements. Sampling in many cities would be equally important to determine if any species shows different adaptive solutions in different cities.

Diagram of research project

I will investigate several species of rodents that have undergone different degrees of adaptation to urban environments in several cities of different sizes, and thus different levels of pollution and urbanization. In each city, animals will be trapped across urban gradients (i.e. there will be two gradients of urbanization, among cities and within cities). For each trapped animal we will calculate the level of pollution and the level of urbanization in the area where the animal was trapped. We will measure comprehensive sets of morphological, physiological (with an emphasis on reproductive physiology, and responses to oxidative stress) and behavioral traits (including the chemical composition of urine and the structure of ultrasonic vocalizations). Using transcriptomics approaches, we will determine whether gene expression in any relevant tissues (e.g. testis) is affected by urbanization and/or pollution. We will also use genomic approaches and common-garden experiments to determine the relative involvement of phenotypic plasticity and genetic evolution in any observed phenotypic changes in urban populations. An extension of this project involves studying the differences in the microbiome between rural and urban populations in several species of rodents, and the stability of those microbiomes under controlled conditions.

1.2 Sperm physiology: evolution of sperm production and function

Another focus of the lab is on evolutionary and ecological sperm physiology, investigating how sperm production and function in different vertebrate species is affected by social and environmental factors, using integrative approaches. For example, we will study (i) how the reproductive potential of different urban species is affected by urbanization; (ii) how pollution may restrict the reproductive responses of aquatic animals to climate change; (iii) what factors affect the cryopreservation of sperm from endangered species for which the use of frozen sperm can be a conservation strategy; and (iv) how in different populations of wide-ranging species sperm production and sperm function change throughout the year, at different latitudes, at different altitudes, and in different types of habitats across the range.

Diagram of research directions

Initially, I will continue my investigations on how sperm competition (a component of sexual selection that takes place when a female mates with two or more males and their spermatozoa compete to fertilize the female’s eggs) drives the evolution of reproductive mechanisms. Using several species of Peromyscus that differ in their mating systems and thus in their levels of sperm competition, I will characterize the relationships between (i) levels of sperm competition; (ii) sperm velocity; (iii) ATP usage and ROS production within spermatozoa; (iv) the cellular mechanisms that minimize oxidative stress in spermatozoa; (v) the differences in genetic expression during spermatogenesis (at different developmental stages and in response to different social stimuli) giving rise to the striking differences in sperm production and sperm function in these species; and (vi) the resilience of spermatozoa to different stressors, such as extracellular ROS, changes in pH or temperature, or the effects of aging. This investigations will elucidate how sexual selection regulates the evolution of sperm traits, and how oxidative damage impacts sperm survival and fertilizing ability.

Diagram of sperm research projects

2. My previous lines of research (which I still want to pursue)

My integrative research bridges several fields, including evolutionary biology, animal behavior, reproductive biology, urban ecology, and chemical ecology, and has been centered around the following interrelated themes:

2.1 An integrative approach to sperm competition in mammals

I have investigated sperm competition at different levels: sperm production, sperm allocation, and sperm evolution. At the level of sperm production, I have found that mammalian species with high sperm competition show a higher proportion of testicular tissue occupied by seminiferous tubules, an increase in the workload of Sertoli cells, and faster rates of spermatogenesis [36]. At the level of sperm allocation, I have shown that males can adjust the number of spermatozoa in their ejaculates under contexts of high sperm competition conveyed by olfactory information from conspecifics [1,5,12,32], and that such adjustments may involve differential muscle contractility of the cauda epididymis and vas deferens [9]. At the level of sperm evolution, I have documented how sperm competition affects the evolution of sperm traits in several mammalian species, addressing the hypothesis that increased sperm competition leads to higher ATP production to fuel higher sperm velocities; and that such heightened metabolism may increase the production of reactive oxygen species (ROS) and thus the risk of oxidative damage [38,40]. In species with high sperm competition, there is a dramatic increase in the proportion of saturated fatty acids in the sperm membrane [38,40], which is biologically relevant, because these fatty acids are the most resistant to oxidative damage. An associated increase in the proportion of spermatozoa with DNA damage suggests that there is an evolutionary trade-off in these species between sperm production and sperm DNA integrity [43]. This increase in sperm DNA damage is a striking finding, as sperm function is predicted to be maximized in species experiencing high levels of sperm competition.

2.2 Learned assortative mating during adulthood

At Cornell University, I studied assortative mating between two closely related species, the Syrian and Turkish hamsters (Mesocricetus spp). I determined that receptive female hamsters show a preference for the odors of conspecific males, and that this preference is regulated by a brain area located between the anterior and posterior medial amygdala [16]. Despite their discriminatory ability, naïve females readily mate with heterospecific males [15,18] and only learn not to do so after long-term exposure to them [21,25,30]. Nevertheless, this learning is temporary and disappears in the absence of further stimuli from heterospecifics [25,27]. Through this work, I showed that the avoidance of interspecific mating is not necessarily an innate or early-learned response and may require learning during adulthood.

2.3 Evolution of olfactory signals in primates

At Duke University and its Lemur Center, I used a comparative approach involving many species of strepsirrhine primates to study the evolution of their chemical signals [22,29,35]. Analyzing the chemical composition of urine and glandular secretions, I determined that there are distinctive chemical patterns, not only between different species, the sexes, individuals, and their various odorant sources (or olfactory points of origin), but also between aspects of these species’ socioecology (e.g. female dominant vs. egalitarian) and activity patterns (i.e., diurnal, nocturnal, vs. cathemeral) [22,29,35,39,49]. I also determined that chemical signals in strepsirrhines evolve at fast rates, following a gradual mode of evolution, which results in highly species- and clade-specific chemical signals [22,29,39]. These data have provided new insights into scent-signal evolution and the origins of cathemerality in lemurs. 

2.4 Integrative urban ecology and evolution

More recently, I have been integrating all my previous experience into a series of interdisciplinary research projects centered around the impacts of urbanization on several species of animals [46,50,51,52,54]. For example, I have started using tardigrades, microscopic invertebrates that are cosmopolitan and resilient to many abiotic stressors, as a new model to study urban adaptation [50,51]. Tardigrades can be found in any city and one can obtain lots of specimens across a city in a question of hours. It is thus possible to sample a large number of cities across the globe. As a result, tardigrades are an excellent model to tease apart the interlinked effects of urbanization and climate change on biodiversity. In collaboration with Breanna Putman (California State Univ. San Bernardino), I have also found that, across many invertebrate and vertebrate species, phenotypic traits (i.e. morphological, physiological, and behavioral traits) differ in separate cities, and that such differences increase with the number of cities investigated, the distance between cities, and the difference in human population density between the cities [55]. These results highlight the importance of investigating the responses of urban animals across an array of cities of different sizes and located in different ecological/climatic regions.

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