Todd H Oakley

University of Hamburg, Hamburg, Hamburg, Germany

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Publications (82)431.51 Total impact

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    ABSTRACT: Research Cite this article: Alexandrou MA et al. 2015 Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae. The competition-relatedness hypothesis (CRH) predicts that the strength of competition is the strongest among closely related species and decreases as species become less related. This hypothesis is based on the assumption that common ancestry causes close relatives to share biological traits that lead to greater ecological similarity. Although intuitively appealing, the extent to which phylogeny can predict competition and co-occurrence among species has only recently been rigorously tested, with mixed results. When studies have failed to support the CRH, critics have pointed out at least three limit-ations: (i) the use of data poor phylogenies that provide inaccurate estimates of species relatedness, (ii) the use of inappropriate statistical models that fail to detect relationships between relatedness and species interactions amidst nonlinearities and heteroskedastic variances, and (iii) overly simplified labora-tory conditions that fail to allow eco-evolutionary relationships to emerge. Here, we address these limitations and find they do not explain why evolutionary relatedness fails to predict the strength of species interactions or probabilities of coexistence among freshwater green algae. First, we construct a new data-rich, transcriptome-based phylogeny of common freshwater green algae that are commonly cultured and used for laboratory experiments. Using this new phylogeny, we re-analyse ecological data from three previously published lab-oratory experiments. After accounting for the possibility of nonlinearities and heterogeneity of variances across levels of relatedness, we find no relationship between phylogenetic distance and ecological traits. In addition, we show that communities of North American green algae are randomly composed with respect to their evolutionary relationships in 99% of 1077 lakes spanning the continental United States. Together, these analyses result in one of the most comprehensive case studies of how evolutionary history influences species interactions and community assembly in both natural and experimental sys-tems. Our results challenge the generality of the CRH and suggest it may be time to re-evaluate the validity and assumptions of this hypothesis.
    Proceedings of the Royal Society B: Biological Sciences 12/2014; 282. · 5.68 Impact Factor
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    ABSTRACT: Background Tools for high throughput sequencing and de novo assembly make the analysis of transcriptomes (i.e. the suite of genes expressed in a tissue) feasible for almost any organism. Yet a challenge for biologists is that it can be difficult to assign identities to gene sequences, especially from non-model organisms. Phylogenetic analyses are one useful method for assigning identities to these sequences, but such methods tend to be time-consuming because of the need to re-calculate trees for every gene of interest and each time a new data set is analyzed. In response, we employed existing tools for phylogenetic analysis to produce a computationally efficient, tree-based approach for annotating transcriptomes or new genomes that we term Phylogenetically-Informed Annotation (PIA), which places uncharacterized genes into pre-calculated phylogenies of gene families.ResultsWe generated maximum likelihood trees for 109 genes from a Light Interaction Toolkit (LIT), a collection of genes that underlie the function or development of light-interacting structures in metazoans. To do so, we searched protein sequences predicted from 30 fully-sequenced genomes and built trees using tools for phylogenetic analysis in the Osiris package of Galaxy (an open-source workflow management system). Next, to rapidly annotate transcriptomes from organisms that lack sequenced genomes, we repurposed a maximum likelihood-based Evolutionary Placement Algorithm (implemented in RAxML) to place sequences of potential LIT genes on to our pre-calculated gene trees. Finally, we implemented PIA in Galaxy and used it to search for LIT genes in 28 newly-sequenced transcriptomes from the light-interacting tissues of a range of cephalopod mollusks, arthropods, and cubozoan cnidarians. Our new trees for LIT genes are available on the Bitbucket public repository (http://bitbucket.org/osiris_phylogenetics/pia/) and we demonstrate PIA on a publicly-accessible web server (http://galaxy-dev.cnsi.ucsb.edu/pia/).Conclusions Our new trees for LIT genes will be a valuable resource for researchers studying the evolution of eyes or other light-interacting structures. We also introduce PIA, a high throughput method for using phylogenetic relationships to identify LIT genes in transcriptomes from non-model organisms. With simple modifications, our methods may be used to search for different sets of genes or to annotate data sets from taxa outside of Metazoa.
    BMC Bioinformatics 11/2014; 15(1):350. · 3.02 Impact Factor
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    ABSTRACT: Despite contingency in life's history, the similarity of evolutionarily convergent traits may represent predictable solutions to common conditions. However, the extent to which overall gene expression levels (transcriptomes) underlying convergent traits are themselves convergent remains largely unexplored. Here, we show strong statistical support for convergent evolutionary origins and massively parallel evolution of the entire transcriptomes in symbiotic bioluminescent organs (bacterial photophores) from two divergent squid species. The gene expression similarities are so strong that regression models of one species' photophore can predict organ identity of a distantly related photophore from gene expression levels alone. Our results point to widespread parallel changes in gene expression evolution associated with convergent origins of complex organs. Therefore, predictable solutions may drive not only the evolution of novel, complex organs but also the evolution of overall gene expression levels that underlie them.
    Proceedings of the National Academy of Sciences of the United States of America. 10/2014;
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    ABSTRACT: Hemocyanin is a copper-containing protein that transports O2 in the hemolymph of many arthropod species. Within the crustaceans, hemocyanin appeared to be restricted to Malacostraca but has recently been identified in Remipedia. Here, we report the occurrence of hemocyanin in ostracods, indicating that this respiratory protein is more widespread within crustaceans than previously thought. By analyses of expressed sequence tags and by RT-PCR, we obtained four full length and nine partial hemocyanin sequences from six of ten investigated ostracod species. Hemocyanin was identified in Myodocopida (Actinoseta jonesi, Cypridininae sp., Euphilomedes morini, Skogsbergia lerneri, Vargula tsujii) and Platycopida (Cytherelloidea californica) but not in Podocopida. We found no evidence for the presence of hemoglobin in any of these ostracod species. Like in other arthropods, we identified multiple hemocyanin subunits (up to six) to occur in a single ostracod species. Bayesian phylogenetic analyses showed that ostracod hemocyanin subunit diversity evolved independently from that of other crustaceans. Ostracod hemocyanin subunits were found paraphyletic, with myodocopid and platycopid subunits forming distinct clades within those of the crustaceans. This pattern suggests that ostracod hemocyanins originated from distinct subunits in the pancrustacean stemline.
    Journal of Molecular Evolution 08/2014; · 2.15 Impact Factor
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    ABSTRACT: Background/Question/Methods Darwin proposed >150-yrs ago that closely related species are more ecologically similar to each other than distantly related species. In turn, he argued closely related species should compete more strongly and be less likely to coexist. For much of the last century, Darwin's hypothesis was taken at face value, and sometimes rose to the status of dogma among those who proposed that conservation and restoration of evolutionary diversity could help maximize the resilience, stability, and ecological functioning of ecosystems. Despite its intuitive appeal, the competition-relatedness hypothesis has received surprisingly little testing. Here we present results from a suite of laboratory and field studies that used freshwater green algae to determine if evolutionary relatedness impacts species interactions, trait similarity, and patterns of co-occurrence. We cultured and sequenced ~60 of the most common species of green algae in lakes across North America to generate a robust molecular phylogeny describing evolutionary relationships. We then (a) performed laboratory competition experiments in which we manipulated the genetic distance among species and measured interaction strengths and niche overlap, (b) examined the evolutionary conservatism of biological traits that underlie interactions, and (c) explored whether patterns of species co-occurrence in real lakes are predicted by relatedness. Results/Conclusions Using lab experiments in which we grew 8 common algal species in mono- and biculture, we fit time series of population dynamics to Lotka-Volterra competition equations to estimate interaction coefficients (alphas). Even though alphas clearly predicted the winners/losers of competition, interaction strengths were independent of phylogenetic distance (F1,23 = 0.56, P = 0.46). We then expanded the species pool and ran experiments using 216 pair-wise combinations of algae, but still found no evidence that phylogenetic distance impacts species relative yields (biomass in mono- vs. biculture, P = 0.19). Following this, we experimentally quantified key biological traits thought to dictate competition for >50 algal species and found the minimum resource levels needed to sustain positive growth (R* values for N, P, light) were not evolutionarily conserved (P > 0.10 for all estimates of Bloomberg's K). Lastly, we examined patterns of species co-occurrence across >1,200 North American lakes and found that the probabilities of co-occurrence were not significantly different than the random expectation of a null model. These diverse empirical studies are all congruent, and suggest the mechanisms of competition may not always be evolutionarily conserved. Therefore, biologists may need to re-evaluate the often assumed generality of Darwin's competition-relatedness hypothesis.
    99th ESA Annual Convention 2014; 08/2014
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    ABSTRACT: Opsins mediate light detection in most animals, and understanding their evolution is key to clarify the origin of vision. Despite the public availability of a substantial collection of well-characterized opsins, early opsin evolution has yet to be fully understood, in large part because of the high level of divergence observed among opsins belonging to different subfamilies. As a result, different studies have investigated deep opsin evolution using alternative datasets and reached contradictory results. Here we integrated the data and methods of three, key, recent studies to further clarify opsin evolution. We show that the opsin relationships are sensitive to outgroup choice; we generate new support for the existence of Rhabdomeric opsins in Cnidaria (e.g. corals and jellyfishes), and show that all comb jelly opsins belong to well-recognized opsin groups (the Go-coupled opsins or the Ciliary opsins), that are also known in Bilateria (e.g. humans, fruit flies, snails and their allies) and Cnidaria. Our results are most parsimoniously interpreted assuming a traditional animal phylogeny where Ctenophora are not the sister group of all the other animals.
    Genome Biology and Evolution 07/2014; · 4.76 Impact Factor
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    ABSTRACT: Phylogenetic tools and 'tree-thinking' approaches increasingly permeate all biological research. At the same time, phylogenetic data sets are expanding at breakneck pace, facilitated by increasingly economical sequencing technologies. Therefore, there is an urgent need for accessible, modular, and sharable tools for phylogenetic analysis.
    BMC Bioinformatics 07/2014; 15(1):230. · 3.02 Impact Factor
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    ABSTRACT: A long-standing hypothesis in ecology and evolutionary biology is that closely related species are more ecologically similar to each other, and therefore, compete more strongly than distant relatives do. A recent hypothesis posits that evolutionary relatedness may also explain the prevalence of mutualisms, with facilitative interactions being more common among distantly related species. Despite the importance of these hypotheses for understanding the structure and function of ecological communities, experimental tests to determine how evolutionary relatedness influences competition and facilitation are still somewhat rare.Here, we report results of a laboratory experiment in which we assessed how competitive and facilitative interactions among eight species of freshwater green algae are influenced by their relatedness. We measured the prevalence of competition and facilitation among 28 pairs of freshwater green algal species that were chosen to span a large gradient of phylogenetic distances. For each species, we first measured its invasion success when introduced into a steady-state population of another resident species. Then, we compared its growth rate when grown alone in monoculture to its growth rate when introduced as an invader. The change in the species’ population growth rate as an invader (sensitivity) is used as a measure of the strength of its interaction with the resident species. A reduced growth rate in presence of another species indicates competition, whereas an increased growth rate indicates facilitation.Although competition between species was more frequent (75% of interactions), facilitation was common (the other 25% of interactions). We found no significant relationship between the phylogenetic distance separating two interacting species and the success of invasion, nor the prevalence or strength of either competition or facilitation. Interspecific interactions depended more on the identity of the species, with certain taxa consistently acting as good or bad competitors/facilitators. These species were not predictable a priori from their positions on a phylogeny.Synthesis. The phylogenetic relatedness of the green algae species used here did not predict the prevalence of competitive and facilitative interactions, rejecting the hypothesis that close relatives compete strongly and contesting recent evidence that facilitation is likely to occur between distant relatives.This article is protected by copyright. All rights reserved.
    Journal of Ecology 05/2014; · 5.69 Impact Factor
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    ABSTRACT: Over 95% of all metazoan (animal) species comprise the “invertebrates,” but very few genomes from these organisms have been sequenced. We have, therefore, formed a “Global Invertebrate Genomics Alliance” (GIGA). Our intent is to build a collaborative network of diverse scientists to tackle major challenges (e.g., species selection, sample collection and storage, sequence assembly, annotation, analytical tools) associated with genome/transcriptome sequencing across a large taxonomic spectrum. We aim to promote standards that will facilitate comparative approaches to invertebrate genomics and collaborations across the international scientific community. Candidate study taxa include species from Porifera, Ctenophora, Cnidaria, Placozoa, Mollusca, Arthropoda, Echinodermata, Annelida, Bryozoa, and Platyhelminthes, among others. GIGA will target 7000 noninsect/nonnematode species, with an emphasis on marine taxa because of the unrivaled phyletic diversity in the oceans. Priorities for selecting invertebrates for sequencing will include, but are not restricted to, their phylogenetic placement; relevance to organismal, ecological, and conservation research; and their importance to fisheries and human health. We highlight benefits of sequencing both whole genomes (DNA) and transcriptomes and also suggest policies for genomic-level data access and sharing based on transparency and inclusiveness. The GIGA Web site (http://giga.nova.edu) has been launched to facilitate this collaborative venture.
    Journal of Heredity 01/2014; 105(1):1-18. · 2.00 Impact Factor
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    ABSTRACT: We describe two new sympatric species of Sarsiellidae from coastal Florida, USA: Eusarsiella bryanjuarezi sp. nov. and Eusarsiella eli sp. nov. We also present a morphological character matrix and maximum likelihood phylogenetic analysis for Sarsiellinae based on original species descriptions, representing 139 sarsiellins (including E. bryanjuarezi and E. eli). While support values across the phylogeny are low, E. bryanjuarezi and E. eli form a sister group pair with 68 % bootstrap support. Our phylogeny also showed support for six other sympatric sister-species pairs, distributed across Sarsiellinae's range, which may be candidates for the study of speciation and niche differentiation. Similar to other analyses of myodocopids, our Sarsiellinae phylogeny recovered only three monophyletic genera: Anscottiella, Cymbicopia, and Chelicopia, indicating that characters used in taxonomy may often be homoplasious. Because of our finding of multiple polyphyletic genera, including the two most speciose genera in the subfamily (Eusarsiella and Sarsiella, the type genus) Sarsiellinae is a strong candidate for taxonomic revision.
    Zootaxa 01/2014; 3802(4):444-58. · 1.06 Impact Factor
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    ABSTRACT: A longstanding concept in community ecology is that closely related species compete more strongly than distant relatives. Ecologists have invoked this 'limiting similarity hypothesis' to explain patterns in the structure and function of biological communities and to inform conservation, restoration, and invasive species management. However, few studies have empirically tested the validity of the limiting similarity hypothesis. Here we report the results of a laboratory microcosm experiment in which we used a model system of 23 common, co-occurring North American freshwater green algae to quantify the strength of 216 pair-wise species' interactions (the difference in population density when grown alone vs. in the presence of another species) along a manipulated gradient of evolutionary relatedness (phylogenetic distance, as the sum of branch lengths separating species on a molecular phylogeny). Interspecific interactions varied widely in these bicultures of phytoplankton, ranging from strong competition (relative yield in poly:monoculture << 1) to moderate facilitation (relative yield > 1). Yet, we found no evidence that the strength of species' interactions was influenced by their evolutionary relatedness. There was no relationship between phylogenetic distance and the average, minimum (inferior competitor), nor maximum (superior competitor) interaction strength across all biculture communities (respectively, P = 0.19; P = 0.17, P = 0.14, N = 428). When we examined each individual species, only 17% of individual species' interactions strengths varied as a function of phylogenetic distance, and none of these relationships remained significant after Bonferoni correction for multiple tests (N = 23). Lastly, when we grouped interactions into five qualitatively different types, the frequency of these types was not related to phylogenetic distance among species pairs (F = 1.63, P = 0.15). Our empirical study adds to several others that suggest the biological underpinnings of competition may not be evolutionarily conserved, and thus, ecologists may need to re-evaluate the previously assumed generality of the limiting similarity hypothesis.
    Ecology 01/2014; · 5.18 Impact Factor
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    ABSTRACT: A growing body of work on the neuroethology of cubozoans is based largely on the capabilities of the photoreceptive tissues, and it is important to determine the molecular basis of their light sensitivity. The cubozoans rely on 24 special purpose eyes to extract specific information from a complex visual scene to guide their behavior in the habitat. The lens eyes are the most studied photoreceptive structures, and the phototransduction in the photoreceptor cells is based on light sensitive opsin molecules. Opsins are photosensitive transmembrane proteins associated with photoreceptors in eyes, and the amino acid sequence of the opsins determines the spectral properties of the photoreceptors. Here we show that two distinct opsins (Tripedalia cystophora-lens eye expressed opsin and Tripedalia cystophora-neuropil expressed opsin, or Tc-leo and Tc-neo) are expressed in the Tripedalia cystophora rhopalium. Quantitative PCR determined the level of expression of the two opsins, and we found Tc-leo to have a higher amount of expression than Tc-neo. In situ hybridization located Tc-leo expression in the retinal photoreceptors of the lens eyes where the opsin is involved in image formation. Tc-neo is expressed in a confined part of the neuropil and is probably involved in extraocular light sensation, presumably in relation to diurnal activity.
    PLoS ONE 01/2014; 9(6):e98870. · 3.53 Impact Factor
  • Journal of Natural History. 01/2014;
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    ABSTRACT: Over 95% of all metazoan (animal) species comprise the “invertebrates,” but very few genomes from these organisms have been sequenced. We have, therefore, formed a “Global Invertebrate Genomics Alliance” (GIGA). Our intent is to build a collaborative network of diverse scientists to tackle major challenges (e.g., species selection, sample collection and storage, sequence assembly, annotation, analytical tools) associated with genome/transcriptome sequencing across a large taxonomic spectrum. We aim to promote standards that will facilitate comparative approaches to invertebrate genomics and collaborations across the international scientific community. Candidate study taxa include species from Porifera, Ctenophora, Cnidaria, Placozoa, Mollusca, Arthropoda, Echinodermata, Annelida, Bryozoa, and Platyhelminthes, among others. GIGA will target 7000 noninsect/nonnematode species, with an emphasis on marine taxa because of the unrivaled phyletic diversity in the oceans. Priorities for selecting invertebrates for sequencing will include, but are not restricted to, their phylogenetic placement; relevance to organismal, ecological, and conservation research; and their importance to fisheries and human health. We highlight benefits of sequencing both whole genomes (DNA) and transcriptomes and also suggest policies for genomic-level data access and sharing based on transparency and inclusiveness. The GIGA Web site (http://giga.nova.edu) has been launched to facilitate this collaborative venture.
    Journal of Heredity 12/2013; 105(1):1-18. · 2.00 Impact Factor
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    ABSTRACT: The squid Euprymna scolopes has evolved independent sets of tissues capable of light detection, including a complex eye and a photophore or 'light organ', which houses the luminous bacterial symbiont Vibrio fischeri. As the eye and light organ originate from different embryonic tissues, we examined whether the eye-specification genes, pax6, eya, six, and dac, are shared by these two organs, and if so, whether they are regulated in the light organ by symbiosis. We obtained sequences of the four genes with PCR, confirmed orthology with phylogenetic analysis, and determined that each was expressed in the eye and light organ. With in situ hybridization (ISH), we localized the gene transcripts in developing embryos, comparing the patterns of expression in the two organs. The four transcripts localized to similar tissues, including those associated with the visual system ∼1/4 into embryogenesis (Naef stage 18) and the light organ ∼3/4 into embryogenesis (Naef stage 26). We used ISH and quantitative real-time PCR to examine transcript expression and differential regulation in postembryonic light organs in response to the following colonization conditions: wild-type, luminescent V. fischeri; a mutant strain defective in light production; and as a control, no symbiont. In ISH experiments light organs showed down regulation of the pax6, eya, and six transcripts in response to wild-type V. fischeri. Mutant strains also induced down regulation of the pax6 and eya transcripts, but not of the six transcript. Thus, luminescence was required for down regulation of the six transcript. We discuss these results in the context of symbiont-induced light-organ development. Our study indicates that the eye-specification genes are expressed in light-interacting tissues independent of their embryonic origin and are capable of responding to bacterial cues. These results offer evidence for evolutionary tinkering or the recruitment of eye development genes for use in a light-sensing photophore.
    Mechanisms of development 10/2013; · 2.83 Impact Factor

Publication Stats

2k Citations
431.51 Total Impact Points

Institutions

  • 2014
    • University of Hamburg
      • Zoological Institute
      Hamburg, Hamburg, Germany
  • 2003–2014
    • University of California, Santa Barbara
      • Department of Ecology, Evolution, and Marine Biology
      Santa Barbara, California, United States
  • 2013
    • University of Michigan
      • School of Natural Resources and Environment
      Ann Arbor, Michigan, United States
    • CSU Mentor
      Long Beach, California, United States
  • 2012
    • University of California, Davis
      • Center for Population Biology
      Davis, CA, United States
  • 2007
    • University of California, Irvine
      • Department of Ecology and Evolutionary Biology
      Irvine, CA, United States
  • 2005
    • Iowa State University
      • Department of Ecology, Evolution and Organismal Biology
      Ames, IA, United States
    • University of Chicago
      • Department of Ecology & Evolution
      Chicago, IL, United States
  • 1998–2004
    • Duke University
      • Department of Biology
      Durham, NC, United States
  • 1999
    • University of Wisconsin - Milwaukee
      • Department of Biological Sciences
      Milwaukee, WI, United States