Our overarching goal is to understand the interaction between the genome and the environment. We have been taking advantage of the excellent infrastructure and generous funding available at OIST to explore how next-generation analytical tools can be used to answer a wide range of fundamental questions in ecology and evolution. As technological advances have equalized the playing field, decreasing disparity of analysis possible for model and non-model systems, we are particularly interested in working with unusual organisms, whose unique biology seems best suited to the questions at hand. Our major research projects are currently focused on understanding the (a) genetic mechanisms involved in social insect caste determination, (b) exploring the genetic consequences of co-evolutionary interactions between symbionts, (c) understanding the interplay between time, geography and genomics structure. We are also interested in developing new next-generation sequencing tools to facilitate our research.
Life on Earth has undergone several major advances in biological complexity. The first and most important development was the origin of organism from single cells. In all multi-cellular organisms some cells give up reproduction, acting as a vehicle for the perpetuation of others. Organisms can form societies, typically fairly flexible affairs made up of unrelated individuals. However, some societies have become ‘superorganisms’, where certain individuals give up reproductive rights for the benefit of a few reproductives. Although multicellularity has evolved only once in the history of life, eusociality evolved repeatedly in many lineages of invertebrates, and even in mammals. Eusocial organisms, such as ants, bees and wasps, are dominant components of almost every ecosystem. Their success is directly due to their social behavior.
There are numerous control mechanisms in single cells in an organism that force them to cooperate. Natural selection, which is near sighted, can select for cells that proliferate at the expense of their well-behaved neighbors and can lead to diseases such as cancer. Consequently, much research has been dedicated to the understanding of cell proliferation control mechanisms. Similarly, there are mechanisms in place to regulate the functioning of superorganisms. The same kinds of conflict that can cause cancer, can also lead to the evolution of aberrant social behavior, such as parasitism and even weirder phenomena. However, we still know relatively little about the genetic underpinnings of eusocial behaviors.
Specifically, we are interested in exploring the genetic basis of caste in ants. We are also interested in using the evolutionary biproducts of caste systems to address more general questions.
Using genetic caste determination (GCD) to understand the switch controlling queen-worker differentiation
Although a newly laid egg can develop either into a queen or a worker in most social insects, in a few species this process is under genetic control. GCD allows us to potentially determine the developmental fate of an individual from early on in life. In collaboration with Chris Smith, we are using the red harvester ant to follow gene expression changes in queen and worker destined individuals from early larval stages into adulthood, in order to understand the development of queen and worker transcriptional networks. We are also working with two other species (Wasmannia auropunctata and Vollenhovia emeryii) to try to identify genes involved in GCD.
Queen-worker differentiation in Diacamma
Unlike most ants, Diacamma do not have true queens, but rather reproductive workers called gamergates. Any worker can become a gamergate after eclosing from a pupa as a ‘callow’ individual. In nests where there is already a gamergate present, this callow ant is attacked and mutilated, becoming a sterile worker. When a gamergate is not present, the callow can become the new gamergate. This system is amenable to a variety of experimental manipulations, and we are currently studying gene changes expression associated with the caste differentiation by the callow. This ant lives in Okinawa, and offers great potential for local fieldwork. We are doing this work in collaboration with Yasukazu Okada.
Evolution of social parasites
Social insect colonies are built on cooperation, and this system is easy to cheat. Many ants have evolved ways to exploit the labor of other species without providing anything in return, a phenomenon termed social parasitism. We are exploring the genetic changes that accompany the evolution of social parasitism in harvester ants.
The symbiosis between attine ants and their cultivar fungi has been a remarkable example of co-evolutionary integration. We have been collaborating with the lab of Ulrich Mueller in a range of studies to understand how such tight interdependence can be maintained over the course of tens of millions of years. We are currently comparing transcriptomes of a range of fungal cultivar species to identify genes that may be crucial in maintaining the symbiosis.
Molecular ecology of snake venoms
Venoms are highly evolved mixtures of proteins made to incapacitate and digest prey. They are analytically tractable by mass spectrometry due to their relatively simple chemical composition. We recently completed a study of the venoms of two local Okinawan pitvipers, the habu (Prothobothrops flavoviridis) and the himehabu (Ovophis okinavensis), comparing gene expression profiles with proteomic profiles inferred through mass spectrometry. In addition to discovering numerous proteins new to snake venoms, this method showed that it is possible to quantitatively measure snake venoms using mass spectrometry. We are in the process of expanding our study to vipers more generally, in order to understand the effects of phylogeny and diet on the evolution of snake venom composition.
Human travel and commerce have made the world a smaller place, and some species have much greater access to new territories than they would normally. A few of these travelers successfully establish in new places, and some of them go on to cause significant ecological and environmental harm. The biology of invasive species, as they are called, is a pressing environmental concern, as well as an opportunity to study ecology and evolution in action. We have been working with an unusual species called the little fire ant (Wasmannia auropunctata) in order to understand what makes some species better invaders, and how species evolve after their introduction.
The little fire ant is a particularly useful species for this line of investigation, since moist invasions are caused by the introduction of a single mated pair. This makes it easy to reconstruct the genetic changes that occurred during the invasion. The little fire ant also has two reproductive forms, one sexual and one clonal, though only the latter is invasive. We are interested in understanding the role reproductive strategy, and genetics play in invasion.
Immigration and natural selection in feral honeybees
Honeybees (Apis mellifera) are crucially important to the security of the world’s food supply by providing pollination services to a wide range of crops. However, bee populations around the world have been crashing for poorly understood reasons. In collaboration with Tom Seeley, we are using museum collections of a bee population from the late 1970s, together with present-day samples to understand the interplay between disease, immigration and natural selection on a feral bee population.
Horizontal gene transfer in bdelloid rotifers
These tiny aquatic invertebrates are reputed to engage in widespread horizontal gene transfer. We are comparing several bdelloid rotifer species to understand the evolutionary dynamics and consequences of this phenomenon.
Host-associated differentiation (HAD) in butterflies
Herbivorous insects rely on suites of genetic adaptation to overcome the defenses of their host plants. Species that feed on several different host plants may have divergent selection on large parts of their genomes in different populations. This may lead to host-associate genomic differentiation between populations, not just in the loci involved in the adaptation, but also at other neutral loci. In extreme cases, HAD may be a precursor to speciation. We are working with two congeneric butterflies (Euphydryas aurinia and E. editha) to try to understand the evolutionary forces that produce host-associated differentiation. The former species has documented suites of adaptive behaviors, but does not show HAD, while the latter shows HAD, but no adaptive suites. We are trying to resolve this apparent paradox, together with Mike Singer. You should check out the excellent advice to graduate students on his web page.
Molecular methods development
Next-generation sequencing of damaged DNA
DNA from many of the most interesting sources comes in the form of short denatured fragments. These fragments are not amenable to many standard molecular approaches, and recalcitrant to sequencing analysis. We have been developing a range of tools short DNA fragments sequenceable using Illumina chemistry. We are particularly interested in non-destructive sampling of museum specimens for next-generation sequencing-based analysis, such as RAD-tagging or whole genome sequencing. However, the generalized approach is useful for most kinds of fragmented DNA, such as formaldehyde fixed paraffin embedded (FFPE) samples (e.g., biopsy tissues), or bisulfite converted samples (e.g. for methylation analysis).