Faculty Research: Todd Oakley

My research involves comparisons of independent evolutionary transitions such as convergence, parallelism, duplication, and homoplasy. Such transitions provide an element of replicability within the singular history of life, and can yield insight into the most general evolutionary questions. For example, when and why do the same molecular or developmental changes underlie similar - though independent - evolutionary changes? What are the fates of duplicated genes, and what causes them to diversify or retain old functions? How can we even determine what isan independent evolutionary event? These questions have driven my research on diverse subjects in evolution. First, I describe my current and planned research on eye evolution. This research focuses on major evolutionary transitions such as the independent origin of an arthropod compound eye and the loss of eyes in females - but not males - of one species. Next, I describe my research on gene duplication in salmonid fishes. I conclude by describing my methodological studies on ancestral state reconstruciton. My interests in gene duplication and phylogenetic ancestral state reconstruction have driven my work on eye evolution.

Eye Evolution in Ostracod Crustaceans

Currently, my major research focus involves developing anew model system for comparative study of the molecular evolution and development of eyes. Eye evolution is paradoxical because tremendous morphological variability is coupled with genetic and developmental stasis across millions of years of evolution. Elucidating "the paradox of eye evolution" by investigating major transitions in eye evolution has far-reaching implications for the evolution of fundamental genetic and developmental processes. I am pioneering molecular analyses of eyes in ostracods, a group of crustaceans well suited for study of eye evolution. Ostracods have two different visual systems: a single median eye, and paired compound eyes. The presence of these eye types is variable in different ostracod taxa, suggesting multiple independent transitions in eye morphology. For example, compound eyes have probably been lost multiple times after transitions to the deep sea or caves. Furthermore, in multiple unrelated species, males have large compound eyes, but females lack these eyes altogether. Ostracods also have made transitions from marine to freshwater - two very different light environments with different demands for vision - on multiple occasions. In addition, ostracods may have evolved compound eyes independently of other arthropods. This "independent eyes" hypothesis was a major focus of my PhD. dissertation at Duke University. One of the most debated issues in arthropod evolution is whether compound eyes evolved once or multiple times. I have found four separate lines of evidence that the compound eyes of ostracods are independently derived. The first evidence is phylogeny. Myodocopids - the only ostracods with compound eyes - are phylogenetically nested within several groups that lack compound eyes. Sequence analyses of 28S and 18S rDNA unequivocally support this result (Fig. 1).

Second, I have documented a recent duplication of visual pigment genes (opsins) coupled with a change to compound eye-specific gene expression. The timing of these events are coincident with the origin of myodocopids and therefore the putative origin of ostracod compound eyes. This gene duplication can be dated phylogenetically without a molecular clock assumption. The recent origin of a compound eye-specific opsin is especially compelling because I cannot detect any other compound eye opsins with older origins. The ancestral absence of compound eye opsins suggests an ancestral absence of compound eyes themselves because all metazoan eyes express opsin. Third, one would expect a unique structure in independently derived organs. The ultrastructure of the facets of ostracod compound eyes deviates from the common arthropod structure of eight retinular cells and four crystalline cone cells. Ostracods have six and two, respectively. Finally, the oldest known fossil ostracod with a compound eye is also the oldest myodocopid. No fossil compound eyes are known from ostracods older than myodocopids. Taken together, these data provide the strongest case yet for the multiple origins of arthropod compound eyes. Developing tools to study the developmental genetics of ostracod vision is the subject of my forthcoming research. This project is to be co-advised by Wen-Hsiung Li andNipam Patel at the University of Chicago. I proposed to examine in ostracods the sequence and expression patterns of four genes highly conserved in fly and vertebrate eye development. The first ostracod species I will examine is Euphilomedes morini because strikingly different developmental programs exist within a single species: males havecompound eyes among the largest of any ostracod, whilefemales have no compound eyes at all. Genes involved ineye development are involved in other developmental processes and I am interested to learn how female E. morini managed to lose eyes during evolution while retaining otherwise normal function. In addition, tools I learn from studying this species can be used in future investigations of other transitions in eye evolution. Examples include the multiple independent losses of eyes in deep sea and cave ostracods and the independent origin of compound eyes in arc clam molluscs and fan worm polychates.

Duplicated Growth Hormone Introns

As I discovered in ostracod opsins, gene duplication can be a major source of evolutionary innovation. Furthermore, duplicated genes provide replicability for the study of molecular evolution because two similar daughter genes evolve separately after duplication. Discovering why some duplicated genes are lost, and why some gain new function is of fundamental importance for understanding evolution. A valuable model group for studying gene duplication in an animal is salmonid fishes (salmon, trout, char, whitefish). Salmonids are ancestrally tetraploid; a common ancestor underwent a genome duplication event about 50-75 million years ago. As a result, many salmonid genes remain duplicated to this day. I examined an intron of one duplicatedgene, growth hormone (GH). Since two copies of the geneare found in all salmonids, a null hypothesis is that both genes should have identical evolutionary histories. I foundthis to be true for phylogenetic histories of the genes: phylogenetic trees based on each duplicate were not significantlydifferent. These trees were informative about several taxonomic controversies. In addition, the GH phylogeny unequivocally rejected monophyly of Atlantic (Salmo) andPacific (Oncorhynchus) salmon/trouts. These genera were previously uncontrovesially considered sister taxa. However, in light of my results, salmonid researchers are now beginning to question this dogma. The phylogenetic relationship is evolutionarily significant because both groups show amazing anadromous behavior - the return of adults to natal rivers for spawning. Although the phylogenetic histories of each GH gene were the same, I found a significant difference in rates of evolution between duplicated GH introns. I attributed thisto differences in natural selection between the introns. This was somewhat unexpected as introns are often thought of as neutrally evolving regions of the genome.

Reconstruction of Ancestral States

My eye evolution research is also intimately tied to my methodological/theoretical research on ancestral state reconstruction, currently one of the most important topics in systematics. Reconstructing ancestral states forms abridge between systematics and many other fields of biology because researchers in diverse fields seek to map characters of interest on to phylogenetic trees. But only recently have researchers begun to seriously question the reliability of character mapping (i.e. Cunningham, Omland and Oakley, 1998). I also added another cautionary tale of ancestral state reconstruction when I conducted research on a known bacteriophage phylogeny created at the University of Texas complete with actual ancestors. I performed the first empirical test of ancestral state reconstruction using continuous character data. I found that phenotypic measures of growth rate evolved in parallel in the experimental system. This led to huge errors in reconstruction of several ancestral nodes. Perhaps most surprisingly, correlative comparative methods fared well, even when using the same data. This provides a clear empirical demonstration that correlative methods may succeed when ancestral state reconstruction does not (Oakley and Cunningham, 2000).In the same study, I used computer simulation to confirm that, in general, trends in character evolution and rapid character evolution cause increased error in estimated ancestral states. Furthermore, terminal character data may not give any clue that trends or rapid character evolution were present during evolution. In the paper describing this work (Oakley and Cunningham, 2000), I suggest that character mapping might be used to generate evolutionary hypotheses rather than test them. My work on compound eyes illustrates exactly one way this might be done in practice - by considering other forms of data, such as genetic, morphological, or paleontological data - in addition to phylogenetic data.

Todd Oakley | Research | Publications | Curriculum Vitae

<< Return to Faculty Page