Primary Research Interests

My main research interest is the molecular evolution of reproductive proteins. Proteins involved in reproduction typically show signs of rapid evolution (Swanson and Vacquier 2002). For example, comparisons of sequence data from Drosophila species show that male reproductive genes are evolving faster than non-reproductive genes (Civetta & Singh 1995; Swanson et al. 2001). Mammalian and marine invertebrate (e.g. abalone and sea urchins) reproductive proteins involved in sperm-egg interactions are also evolving rapidly by adaptive evolution (Makalowski & Boguski 1998; Swanson et al. 2003; Hellberg et al. 2000; Hellberg & Vacquier 1999; Lee & Vacquier 1992; Metz et al. 1998a; Yang et al. 2000). The adaptive mechanism for rapid evolution of reproductive proteins has not been directly identified, but potential mechanisms include co-evolutionary processes that result from sexual selection, sexual conflict, immune defense, and self vs. non-self recognition. Given that many reproductive proteins are involved in interactions (either directly or indirectly) with the opposite sex, insight into the evolutionary mechanisms will be gained by the integration of genetic, experimental, and theoretical studies on both male and female reproductive proteins (Panhuis et al. 2006, in press).

In Drosophila, a group of reproductive proteins known as the accessory gland proteins (Acps) are expressed by males and enter the female reproductive tract upon mating. Several Acp proteins have been shown to affect sperm storage, female remating receptivity, female longevity, and female egg laying rate (Wolfner 1997). The effect of male Acps on female fitness suggest females should evolve interacting proteins to Acps and play a role in the processes relating to male reproductive success. There is evidence that females are a key player in determining male reproductive success, both in sperm competition and in the fecundity of a single mating (Price 1997; Clark & Begun 1998; Clark et al 1999; Panhuis & Nunney unpubl.). However, there is still little information on the interacting female reproductive proteins. If we are to obtain a better understanding of the evolution of Acps and reproductive proteins in general, the identity of interacting male-female reproductive proteins must be established. With regards to this research I have recently completed a post-doctoral fellowship at the University of Washington in Willie Swanson’s laboratory (http://www.gs.washington.edu/labs/swanson/index.htm). In the Swanson lab I initiated a project aimed at identifying female reproductive proteins using insect cell expression of candidate female genes (identified by Swanson et al. 2004) and fluorescent assisted cell sorting (FACS) technology. In addition to this work, I completed a population genetics analysis on nine candidate female reproductive genes (identified by Swanson et al. 2004). Using polymorphism surveys of positive selection (e.g. Tajima’s D) and divergence analyses (PAML), I found that five out of the nine genes surveyed exhibit signs of positive selection (Panhuis and Swanson, in prep.). This is similar to an initial survey of several different candidate genes by Swanson et al. (2004) and suggests that these genes may be likely candidates for encoding molecules that interact with male reproductive proteins after mating (Swanson et al. 2004; Panhuis and Swanson in prep). Follow-up functional analyses will shed light on their potential role in male-female interactions.

I am currently involved in two post-doctoral projects at UCR. My first project, in collaboration with David Reznick examines the molecular evolution of the placenta in poecillid fish. Fish in the genus Poeciliopsis (Poeciliidae) exhibit a range in live-bearing from lecithotrophic species that retain eggs after fertilization with no further maternal provisioning to matrotrophic species that exhibit varying amounts of maternal provisioning after fertilization (Thibault & Sxhultz 1978; Reznick et al. 2002). The relative extent of maternal provisioning is quantified by a maternal index (MI), which is the ratio of the dry weight of the offspring at birth to the dry weight of the egg at fertilization (Reznick et al. 2002). Lecithotrophic species have a MI less than one, while matrotrophic species range from around 5 to greater than 100. The elaborate structures that facilitate a large MI in matrotrophic species are maternal and embryonic tissues that exchange nutrients between the mother and the developing embryo. These tissues are termed the pseudo-placenta (Turner 1940) or the follicular placenta (Knight et al. 1985; Wourms et al.1988) given their similar function to mammalian placentas. Across the range of species there is great variation in the specialization of this tissue with species having little to no specialized tissue to those with highly elaborate follicular placentas (Reznick et al. 2002). Recent work by Reznick et al. (2002) has shown that the placenta has evolved independently at least three times in Poeciliopsis and can evolve in 750,000 years or less. My project is to elaborate on our understanding of the evolution of the placenta through comparative, phylogenetic work that incorporates other species of Poeciliopsis and other genera of fish characterized by their degree of MI. My main goal will be to collect sequence data of several mitochondrial genes from the different fish and generate a phylogeny. These results will shed additional light on the evolution of this complex reproductive trait.

In addition to this work I will initiate a project that will develop genomic resources for the comparative study of the evolution of the placenta. The goal will be to create cDNA libraries from the specialized maternal and embryonic tissues associated with the placenta in species with a well-developed placenta and in one or more close relatives that either lack the placenta or has one in intermediate stages of development. Since the placenta evolved independently three times in Poeciliidae, interesting candidate genes can be identified in association with each origin.

My second post-doctorate project is in collaboration with Daphne Fairbairn and Rich Cardullo. The aim of the project is to determine the function and molecular evolution of sperm and reproductive proteins in the water strider, Aquarius remigis. Water striders have been an important model system for the study of sexual selection and sexual conflict, specifically the role of sexual conflict in altering male and female reproductive morphology. However, little is known about post-mating male-female interactions and the potential role of sexual conflict in the evolution of reproductive proteins and sperm in this system. A. remigis is a good candidate species for addressing questions about the role of sexual conflict in the evolution of sperm and male reproductive proteins. In this species females mate multiply and potentially store sperm from multiple males creating an opportunity for sperm competition and conflict between the sexes in remating rate. Furthermore, A. remigis has remarkably long sperm with an unusually large arcrosome, which may be important in male-female post-mating interactions. Our goal is to use biochemical and microscopy to detail the morphology of the sperm, determine an acrosome reaction, and characterize the acrosomal proteins. Later analyses will include the role of sperm length in male-female post-mating interactions and sperm competition.