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Streelman, J. Todd

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    The evolution of simple versus complex biomechanical systems
    (Georgia Institute of Technology, 2013-01-31) Streelman, J. Todd
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    An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws
    (Georgia Institute of Technology, 2009-02-10) Fraser, Gareth J. ; Hulsey, C. Darrin ; Bloomquist, Ryan F. ; Uyesugi, Kristine ; Manley, Nancy R. ; Streelman, J. Todd
    Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hoxpositive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.
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    Natural selection governs local, but not global, evolutionary gene coexpression networks in Caenorhabditis elegans
    (Georgia Institute of Technology, 2008-11-13) Jordan, I. King ; Katz, Lee S. ; Denver, Dee R. ; Streelman, J. Todd
    Background. Large-scale evaluation of gene expression variation among Caenorhabditis elegans lines that have diverged from a common ancestor allows for the analysis of a novel class of biological networks – evolutionary gene coexpression networks. Comparative analysis of these evolutionary networks has the potential to uncover the effects of natural selection in shaping coexpression network topologies since C. elegans mutation accumulation (MA) lines evolve essentially free from the effects of natural selection, whereas natural isolate (NI) populations are subject to selective constraints. Results. We compared evolutionary gene coexpression networks for C. elegans MA lines versus NI populations to evaluate the role that natural selection plays in shaping the evolution of network topologies. MA and NI evolutionary gene coexpression networks were found to have very similar global topological properties as measured by a number of network topological parameters. Observed MA and NI networks show node degree distributions and average values for node degree, clustering coefficient, path length, eccentricity and betweeness that are statistically indistinguishable from one another yet highly distinct from randomly simulated networks. On the other hand, at the local level the MA and NI coexpression networks are highly divergent; pairs of genes coexpressed in the MA versus NI lines are almost entirely different as are the connectivity and clustering properties of individual genes. Conclusion. It appears that selective forces shape how local patterns of coexpression change over time but do not control the global topology of C. elegans evolutionary gene coexpression networks. These results have implications for the evolutionary significance of global network topologies, which are known to be conserved across disparate complex systems.
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    A periodic pattern generator for dental diversity
    (Georgia Institute of Technology, 2008-07-14) Fraser, Gareth J. ; Bloomquist, Ryan F. ; Streelman, J. Todd
    Background: Periodic patterning of iterative structures is a fundamental process during embryonic organization and development. Studies have shown how gene networks are employed to pattern butterfly eyespots, fly bristles and vertebrate epithelial appendages such as teeth, feathers, hair and mammary glands. Despite knowledge of how these features are organized, little is known about how diversity in periodic patterning is generated in nature. We address this problem through the molecular analysis of oral jaw dental diversity in Lake Malawi cichlids, where closely related species exhibit from 1 to 20 rows of teeth, with total teeth counts ranging from around 10 to 700. Results: We investigate the expression of conserved gene networks (involving bmp2, bmp4, eda, edar, fgf8, pax9, pitx2, runx2, shh and wnt7b) known to pattern iterative structures and teeth in other vertebrates. We show that spatiotemporal variation in expression pattern reflects adult morphological diversity among three closely related Malawi cichlid species. Combinatorial epithelial expression of pitx2 and shh appears to govern the competence both of initial tooth sites and future tooth rows. Epithelial wnt7b and mesenchymal eda are expressed in the inter-germ and inter-row regions, and likely regulate the spacing of these shh-positive units. Finally, we used chemical knockdown to demonstrate the fundamental role of hedgehog signalling and initial placode formation in the organization of the periodically patterned cichlid dental programme. Conclusion: Coordinated patterns of gene expression differ among Malawi species and prefigure the future-ordered distribution of functional teeth of specific size and spacing. This variation in gene expression among species occurs early in the developmental programme for dental patterning. These data show how a complex multi-rowed vertebrate dentition is organized and how developmental tinkering of conserved gene networks during iterative pattern formation can impact upon the evolution of trophic novelty.
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    Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids
    (Georgia Institute of Technology, 2008-07-10) Loh, Yong-Hwee E. ; Katz, Lee S. ; Mims, Meryl C. ; Kocher, Thomas D. ; Yi, Soojin V. ; Streelman, J. Todd
    Background: Cichlid fish from East Africa are remarkable for phenotypic and behavioral diversity on a backdrop of genomic similarity. In 2006, the Joint Genome Institute completed low coverage survey sequencing of the genomes of five phenotypically and ecologically diverse Lake Malawi species. We report a computational and comparative analysis of these data that provides insight into the mechanisms that make closely related species different from one another. Results: We produced assemblies for the five species ranging in aggregate length from 68 to 79 megabase pairs, identified putative orthologs for more than 12,000 human genes, and predicted more than 32,000 cross-species single nucleotide polymorphisms (SNPs). Nucleotide diversity was lower than that found among laboratory strains of the zebrafish. We collected around 36,000 genotypes to validate a subset of SNPs within and among populations and across multiple individuals of about 75 Lake Malawi species. Notably, there were no fixed differences observed between focal species nor between major lineages. Roughly 3% to 5% of loci surveyed are statistical outliers for genetic differentiation (FST) within species, between species, and between major lineages. Outliers for FST are candidate genes that may have experienced a history of natural selection in the Malawi lineage. Conclusion: We present a novel genome sequencing strategy, which is useful when evolutionary diversity is the question of interest. Lake Malawi cichlids are phenotypically and behaviorally diverse, but they appear genetically like a subdivided population. The unique structure of Lake Malawl cichlid genomes should facilitate conceptually new experiments, employing SNPs to identity genotype-phenotype association, using the entire species flock as a mapping panel.
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    Visual sensitivities tuned by heterochronic shifts in opsin gene expression
    (Georgia Institute of Technology, 2008-05-23) Carleton, Karen L. ; Spady, Tyrone C. ; Streelman, J. Todd ; Kidd, Michael R. ; McFarland, William N. ; Loew, Ellis R.
    Background: Cichlid fishes have radiated into hundreds of species in the Great Lakes of Africa. Brightly colored males display on leks and vie to be chosen by females as mates. Strong discrimination by females causes differential male mating success, rapid evolution of male color patterns and, possibly, speciation. In addition to differences in color pattern, Lake Malawi cichlids also show some of the largest known shifts in visual sensitivity among closely related species. These shifts result from modulated expression of seven cone opsin genes. However, the mechanisms for this modulated expression are unknown. Results: In this work, we ask whether these differences might result from changes in developmental patterning of cone opsin genes. To test this, we compared the developmental pattern of cone opsin gene expression of the Nile tilapia, Oreochromis niloticus, with that of several cichlid species from Lake Malawi. In tilapia, quantitative polymerase chain reaction showed that opsin gene expression changes dynamically from a larval gene set through a juvenile set to a final adult set. In contrast, Lake Malawi species showed one of two developmental patterns. In some species, the expressed gene set changes slowly, either retaining the larval pattern or progressing only from larval to juvenile gene sets (neoteny). In the other species, the same genes are expressed in both larvae and adults but correspond to the tilapia adult genes (direct development). Conclusion: Differences in visual sensitivities among species of Lake Malawi cichlids arise through heterochronic shifts relative to the ontogenetic pattern of the tilapia outgroup. Heterochrony has previously been shown to be a powerful mechanism for change in morphological evolution. We found that altering developmental expression patterns is also an important mechanism for altering sensory systems. These resulting sensory shifts will have major impacts on visual communication and could help drive cichlid speciation.
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    Hybridization produces novelty when the mapping of form to function is many to one
    (Georgia Institute of Technology, 2008-04-28) Parnell, Nicholas F. ; Hulsey, C. Darrin ; Streelman, J. Todd
    Background: Evolutionary biologists want to explain the origin of novel features and functions. Two recent but separate lines of research address this question. The first describes one possible outcome of hybridization, called transgressive segregation, where hybrid offspring exhibit trait distributions outside of the parental range. The second considers the explicit mapping of form to function and illustrates manifold paths to similar function (called many to one mapping, MTOM) when the relationship between the two is complex. Under this scenario, functional novelty may be a product of the number of ways to elicit a functional outcome (i.e., the degree of MTOM). We fuse these research themes by considering the influence of MTOM on the production of transgressive jaw biomechanics in simulated hybrids between Lake Malawi cichlid species. Results: We characterized the component links and functional output (kinematic transmission, KT) of the 4-bar mechanism in the oral jaws of Lake Malawi cichlids. We demonstrated that the input and output links, the length of the lower jaw and the length of the maxilla respectively, have consistent but opposing relationships with KT. Based on these data, we predicted scenarios in which species with different morphologies but similar KT (MTOM species) would produce transgressive function in hybrids. We used a simple but realistic genetic model to show that transgressive function is a likely outcome of hybridization among Malawi species exhibiting MTOM. Notably, F2 hybrids are transgressive for function (KT), but not the component links that contribute to function. In our model, transgression is a consequence of recombination and assortment among alleles specifying the lengths of the lower jaw and maxilla. Conclusion: We have described a general and likely pervasive mechanism that generates functional novelty. Simulations of hybrid offspring among Lake Malawi cichlids exhibiting MTOM produce transgressive function in the majority of cases, and at appreciable frequency. Functional transgression (i) is a product of recombination and assortment between alleles controlling the lengths of the lower jaw and the maxilla, (ii) occurs in the absence of transgressive morphology, and (iii) can be predicted from the morphology of parents. Our genetic model can be tested by breeding Malawi cichlid hybrids in the laboratory and examining the resulting range of forms and Malawi cichlid hybrids in the laboratory and examining the resulting range of forms and functions.
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    Evolution, what it is and what is isn't
    (Georgia Institute of Technology, 2006-06-03) Ludovice, Peter J. ; Hunt, William D. ; Streelman, J. Todd
    Evolution, what it is and what is isn't with Georgia Tech Biology Professor, Todd Streelman