The main focus of the laboratory is to use a molecular ecology approach to elucidate the biodiversity, ecology, and evolution of parasites. Because parasites are small and inhabit inconspicuous places (e.g., the gut of a vertebrate), it is difficult and sometimes impossible to directly observe the population dynamics of parasites. However, the use of genetic markers and population genetics theory allows the indirect inference of many population demographic processes such as dispersal, mating dynamics, and transmission patterns. Ongoing research efforts address both basic and applied questions spanning the intersections of genetics, evolution, and ecology. We largely focus on macroparasites (e.g., nematodes, flatworms), but are open to other parasitic systems.

If you are a prospective student interested in working in the lab, or have questions about our research, feel free to contact us.

Ongoing projects include:

1. Evolutionary population genomics of host defense and parasite counter-defense
2. Evolutionary dynamics of parasite life cycle complexity
3. The role of parasite ecology in shaping parasite evolution

Evolutionary population genomics of host defense and parasite counter-defense

The direct interplay between parasites and their hosts enables reciprocal selective pressures that can shape underlying genetic variation in both parasites and their hosts. Indeed, genetic diversity and/or specific alleles at host major histocompatibility complex (MHC) genes have been found to be associated with patterns of parasite infection. Nonetheless, there remain key gaps in elucidating the extent to which reciprocal selection shapes the evolution of parasite-host interactions. Notice that I list parasite first rather than the typical phrase “host-parasite”. The reason is that the gaps are largely on the parasite side. In particular, when it comes to metazoan parasites, accurate parasite species identification and hence, accurate parasite quantification is scant in studies looking at host immunity associations to parasite infections. Moreover, host-mediated selection on the genetic diversity of helminth counter-defense loci is rarely considered.

Are goals are to remedy these gaps by using a model system we developed. Over the past 20 years, we have studied the basic natural history and population genetics of the Mediterranean gecko, Hemidactylus turcicus, and its helminth fauna (specifically the tapeworm Oochoristica javaenesis and the pentastome Raillietiella indica). Our system can address both the effects of parasite-mediated selection on host defense loci and host-mediated selection on putative helminth counter-defense loci. We have draft genome data for the gecko and the tapeworm (with near future plans for the pentastome). These genomic data will serve as the foundation to study the evolution of host immune loci and parasite loci that enable evasion or modulation of host immunity via various approaches: bioinformatics, transcriptomics, phylogenomics, and population genomics. Additional topics of study will include the effects of inbreeding on genome evolution (the tapeworm has high rates of self- and kin-mating), evolution of gene families in both the host and parasites, and genomics of invasive species (the host and the above two parasites are exotic species in the U.S.A.).

Collaborators on the project include Dr. Heath Blackmon (Biology Dept, Texas A&M) and Dr. Michael Criscitiello (Department of Veterinary Pathobiology, Texas A&M).

Evolutionary dynamics of parasite life cycle complexity

Evolutionary change in life cycle complexity is of central importance in parasitology. Addition or removal of a host from a parasite’s life cycle is not a trivial evolutionary event; such transitions can have major consequences for parasite transmission, behavior, physiology, development, and mating systems. My lab is interested in the evolutionary origins and outcomes of changes in life cycle complexity. We use the trematode genus Alloglossidium as a model system because among the species, there is variation in final host species (catfishes, crustaceans, and leeches) and in host number needed to complete the life cycle (2 or 3 hosts). Foundational taxonomic work has stemmed from this work (e.g., Kasl et al. 2014) as well as key phylogenetic work. Studying the causes and consequences of complex life changes hinges on knowing the evolutionary order of life cycle transitions, which in itself, requires data on phylogenetic relationships among species that differ in life cycle patterns. Our molecular phylogeny of the genus Alloglossidium (Kasl et al. 2018) represents a key contribution to this field. A novel study testing the evolutionary theory of sex allocation also emerged from our work on the genus Alloglossidium. Kasl et al. (2015) showed how a life cycle change, precocious maturation in a 2nd intermediate host, could have the consequential impact of causing reproductive trait evolution, i.e., changes in sex allocation. Our study represents 1 of only 3 studies on animal hermaphrodites (and the first on a parasite) to test among-population evolution in sex allocation as a response to varying mating systems. This study not only shows a consequence of a life cycle change, but also has the broader value of showing how the evolution of one trait can affect the evolution of another trait.

We are currently addressing the big picture topic of complex life cycle evolution itself. Specifically, we are testing the mating system model for the evolution of complex life cycles. This model proposes that parasite mating systems maintain or generate complex life cycles. A key model assumption is that complex life cycles for hermaphroditic parasites increase the probability of outcrossing with unrelated individuals, and thus reduce inbreeding relative to a simpler life cycle. Also, a key prediction of the model is that because inbreeding is greater in a simpler life cycle, a shorter life cycle will only be favored when the fitness of inbred offspring is equal to or greater than outbred offspring, i.e., there is no inbreeding depression. To test the mating system model, we are addressing 2 questions using comparative population genetics among species of Alloglossidium: 1) Does a reduction in host number change the mating system? 2) Given a life cycle change that does cause more inbreeding, is inbreeding depression a necessary outcome? My PhD student Jenna Hulke is spearheading this work.

The role of parasite ecology in shaping parasite evolution:

Inbreeding is a critical evolutionary mechanism that can magnify genetic drift and alter selection efficiency. Indeed, parasite inbreeding has been regarded as a means of affecting parasite diversification, host-parasite coevolution, and drug resistance evolution. Yet, empirical data are lacking on levels of parasite inbreeding and fundamental aspects about how parasite life histories impact inbreeding remain to be addressed. Work in my lab has laid the conceptual foundation for understanding how transmission, a central element of parasite ecology, could impact inbreeding (Gorton et al. 2012), and established Oochoristica javaensis, a tapeworm of the Mediterranean gecko, as a model system to explore these dynamics (Detwiler & Criscione 2011; Detwiler & Criscione 2014).

Two of our studies are pioneering by providing novel insights and approaches to studying parasite mating systems and inbreeding in natural systems. In Detwiler et al. (2017), we devised an explicit framework to test how infection intensities (the number parasites in a host) could shape primary selfing rates, and provided innovative formulas that enabled the first-ever, field-collected estimates of individual flatworm selfing-rates. We found an inverse power relationship between infection intensities and individual parasite selfing rates. This result is significant because it indicates that the distribution of parasites among hosts, an emergent ecological property of the transmission process, can be a key driver in shaping the primary mating system, and hence the level of inbreeding in the parasite population. We also highlighted how density-dependent fecundity (a.k.a., the classic parasitological phenomenon of “crowding”) could enhance the population selfing rate. In Detwiler & Criscione (2017), we developed unique analyses, which make use of pedigree reconstruction data, to test how another aspect of transmission could lead to biparental inbreeding. In particular, we provided a novel test of co-sibling transmission and derived a new metric to estimate kin-mating rates. Also, existing parasite studies rely on an inbreeding-based, assumption-heavy, indirect method to estimate a mating system. Our study provides a new and more appropriate approach to first independently estimate the mating system components (selfing and kin-mating) and then asks if these account for the levels of observed population inbreeding.

To fully appreciate the significance of our above work, some historical context is needed. Spanning 5 decades of research on the evolutionary biology of hermaphroditic mating systems, there are field-based, direct selfing rate estimates for over 350 plant species. Among the 130,000 estimated flatworm parasites (of which the vast majority are hermaphroditic), we have provided the first nature-derived, direct selfing-rate and kin-mating estimates. Our studies are not just reports, but rather conducted in the context of elucidating how the ecology drives the mating system, and therefore the evolution of the parasites. We have ongoing work that examines the factors that shape parasitic flatworm mating systems in nature.