A4

Mathematical modeling of interactions in evolving metaorganisms

Why do individuals from different taxonomic groups and even kingdoms of life interact with each other within a metaorganism in a generally beneficial way and thereby form a unit of selection? This question is one of the most fascinating, unresolved mysteries in current evolutionary biology. The reason is that selection at the individual level should usually be strongest for an evolving population, because at this level phenotypic variation directly translates into fitness differences among the individuals. At the level of the entire community, the same variations merge into an average value of fitness, possibly slowing down the response to selection at the community level.

Mathematical models can help us understand the selective conditions that favour beneficial interactions within the metaorganism. This project aims at establishing mathematical models based on empirical data obtained from two simple experimental systems, the Hydra and the C. elegans metaorganisms, which both serve to describe the interaction between different microbe types (bacteria, bacteriophages) and between these microbes and their host. The models will be used to understand the dynamics of the microbial interactions, i.e. the change in relative and absolute abundances of microbes over time, and also the resulting effects on fitness and other life-history functions of the metaorganism.

The project will rely on a close collaboration between experimental and theoretical groups. During the development of the mathematical models, which will be an abstraction and simplification of the biological reality, we will test important basic model assumptions and thereafter further expand the model in an iterative procedure between theory and experiments. The proposed project will prepare the ground for applying similar theoretical approaches to other research projects of the CRC 1182.

Researchers

Janina Lange

PhD Candidate, Associated Junior Researcher
Kiel University Zoological Institute

Publications

2017

Discovering Complete Quasispecies in Bacterial Genomes.

Bertels F, Gokhale C S, Traulsen A (2017); Genetics., 206(2). doi: 10.1534/genetics.117.201160

Ribosome reinitiation can explain length-dependent translation of messenger RNA.

Rogers D W, Böttcher M A, Traulsen A, Greig D (2017); PLoS Comput Biol., 13(6):e1005592. doi: 10.1371/journal.pcbi.1005592

FeaturedAlternative evolutionary paths to bacterial antibiotic resistance cause distinct collateral effects.

Barbosa C, Trebosc V, Kemmer C, Rosenstiel P, Beardmore R, Schulenburg H, Jansen G (2017); Mol Biol Evol., doi: 10.1093/molbev/msx158

The Natural Biotic Environment of Caenorhabditis elegans.

Schulenburg H, Félix M A (2017); Genetics., 206(1):55-86. doi: 10.1534/genetics.116.195511

Highly potent host external immunity acts as a strong selective force enhancing rapid parasite virulence evolution.

Rafaluk C, Yang W, Mitschke A, Rosenstiel P, Schulenburg H, Joop G (2017); Environ Microbiol., 19(5):2090-2100. doi: 10.1111/1462-2920.13736

Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae.

Greenwood J M, Milutinović B, Peuß R, Behrens S, Esser D, Rosenstiel P, Schulenburg H, Kurtz J (2017); BMC Genomics., 18(1):329. doi: 10.1186/s12864-017-3705-7

Detecting truly clonal alterations from multi-region profiling of tumours.

Werner B, Traulsen A, Sottoriva A, Dingli D (2017); Sci Rep., 7:44991. doi: 10.1038/srep44991

Caenorhabditis elegans as a model for microbiome research.

Zhang F, Berg M, Dierking K, Félix M A, Shapira M, Samuel B, Schulenburg H (2017); Front. Microbiol., 8:485. doi: 10.3389/fmicb.2017.00485

Evolutionary games on cycles with strong selection.

Altrock P M, Traulsen A, Nowak M A (2017); Phys Rev E., 95(2-1):022407. doi: 10.1103/PhysRevE.95.022407

Back to the Basics: Cnidarians Start to Fire.

Bosch T C, Klimovich A, Domazet-Lošo T, Gründer S, Holstein T W, Jékely G, Miller D J, Murillo-Rincon A P, Rentzsch F, Richards G S, Schröder K, Technau U, Yuste R (2017); Trends Neurosci., 40(2):92-105. doi: 10.1016/j.tins.2016.11.005

2016

Emerging Sponge Models of Animal-Microbe Symbioses.

Pita L, Fraune S, Hentschel U (2016); Front Microbiol., 7:2102. doi: 10.3389/fmicb.2016.02102

Only the combination of mathematics and agent-based simulations can leverage the full potential of evolutionary modeling: Comment on “Evolutionary game theory using agent-based methods” by C. Adami, J. Schossau and A. Hintze.

Hilbe C, Traulsen A (2016); Phys Life Rev., 19:29-31. doi: 10.1016/j.plrev.2016.10.004

Exact numerical calculation of fixation probability and time on graphs.

Hindersin L, Möller M, Traulsen A, Bauer B (2016); Biosystems., 150:87-91. doi: 10.1016/j.biosystems.2016.08.010

FRT – FONDATION RENE TOURAINE: An International Foundation For Dermatology.

Bosch T C, Zengler K, Naik S, Biedermann T, Kong H H, Loser K, Brüggeman H, Calleawert C, Lambert J, Van de Wiele T (2016); Exp Dermatol., 25(11):917-932. doi: 10.1111/exd.13160

The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra.

Schröder K, Bosch T C (2016); MBio., 7(6):e01184-16. doi: 10.1128/mBio.01184-16

Transitioning from Microbiome Composition to Microbial Community Interactions: The Potential of the Metaorganism Hydra as an Experimental Model.

Deines P, Bosch T C G (2016); Front. Microbiol., 7:1610. doi: 10.3389/fmicb.2016.01610

Response to the Editor: On the Growth of Hematopoietic Stem Cells and Childhood Leukemias.

Werner B, Traulsen A, Dingli D (2016); Stem Cells., 34(10):2610. doi: 10.1002/stem.2469

Should tissue structure suppress or amplify selection to minimize cancer risk?

Hindersin L, Werner B, Dingli D, Traulsen A (2016); Biol Direct., 11:41. doi: 10.1186/s13062-016-0140-7

Using Nematostella vectensis to Study the Interactions between Genome, Epigenome, and Bacteria in a Changing Environment.

Fraune S, Forêt S, Reitzel A M (2016); Front. Mar. Sci., 3:148. doi: 10.3389/fmars.2016.00148

Evolutionary Games of Multiplayer Cooperation on Graphs.

Peña J, Wu B, Arranz J, Traulsen A (2016); PLoS Comput Biol., 12(8):e1005059. doi: 10.1371/journal.pcbi.1005059

ABSSeq: a new RNA-Seq analysis method based on modelling absolute expression differences.

Yang W, Rosenstiel P C, Schulenburg H (2016); BMC Genomics., 17:541. doi: 10.1186/s12864-016-2848-2

Host-parasite coevolution-rapid reciprocal adaptation and its genetic basis.

Kurtz J, Schulenburg H, Reusch T B (2016); Zoology (Jena), 119(4):241-3. doi: 10.1016/j.zool.2016.06.011

Evolving synergetic interactions.

Wu B, Arranz J, Du J, Zhou D, Traulsen A (2016); J R Soc Interface., 13(120):pii:20160282. doi: 10.1098/rsif.2016.0282

How Life History Can Sway the Fixation Probability of Mutants.

Li X Y, Kurokawa S, Giaimo S, Traulsen A (2016); Genetics., 203(3):1297-313. doi: 10.1534/genetics.116.188409

Response of bacterial colonization in Nematostella vectensis to development, environment and biogeography.

Mortzfeld B M, Urbanski S, Reitzel A M, Künzel S, Technau U, Fraune S (2016); Environ Microbiol., 18(6):1764-81. doi: 10.1111/1462-2920.12926

GATA transcription factor as a likely key regulator of the Caenorhabditis elegans innate immune response against gut pathogens.

Yang W, Dierking K, Rosenstiel P C, Schulenburg H (2016); Zoology, doi: 10.1016/j.zool.2016.05.013

Association between clinical antibiotic resistance and susceptibility of Pseudomonas in the cystic fibrosis lung.

Jansen G, Mahrt N, Tueffers L, Barbosa C, Harjes M, Adolph G, Friedrichs A, Krenz-Weinreich A, Rosenstiel P, Schulenburg H (2016); Evol Med Publ Health, doi: 10.1093/emph/eow016

Antimicrobial effectors in the nematode C. elegans – an outgroup to the Arthropoda.

Dierking K, Yang W, Schulenburg H (2016); Phil Trans R Soc Lond B., 371. doi:

The native microbiome of the nematode Caenorhabditis elegans: Gateway to a new host-microbiome model.

Dirksen P, Marsh SA, Braker I, Heitland N, Wagner S, Nakad R, Mader S, Petersen C, Kowallik V, Rosenstiel P C, Felix M A, Schulenburg H (2016); BMC Biology, 14:38. doi:10.1186/s12915-016-0258-1

Coevolutionary interactions between farmers and mafia induce host acceptance of avian brood parasites.

Abou Chakra M, Hilbe C, Traulsen A (2016); R Soc Open Sci., 3(5):160036. doi: 10.1098/rsos.160036

Understanding why we age and how: Evolutionary biology meets different model organisms and multi-level omics.

Gilson E, Bosch T C G (2016); Meeting report on “Comparative Biology of Aging”, Roscoff, October 12-16, 2015. BioEssays, 38(6):494-97. doi: 10.1002/bies.201600049

Contrasting invertebrate immune defense behaviors caused by a single gene, the Caenorhabditis elegans neuropeptide receptor gene npr-1.

Nakad R, Snoek L B, Yang W, Ellendt S, Schneider F, Mohr T G, Rösingh L, Masche A C, Rosenstiel P C, Dierking K, Kammenga J E, Schulenburg H (2016); BMC Genomics, 17: 280. doi: 10.1186/s12864-016-2603-8

Eco-evolutionary dynamics in a coevolving host-virus system.

Frickel J, Sieber M, Becks L (2016); Ecol Lett., 19(4):450-9. doi: 10.1111/ele.12580

Getting the Hologenome Concept Right: An Eco-Evolutionary Framework for Hosts and Their Microbiomes.

Theis K R, Dheilly N M, Klassen J L, Brucker R M, Baines J F, Bosch T C, Cryan J F, Gilbert S F, Goodnight C J, Lloyd E A, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein S R (2016); mSystems., 1(2).pii:e00028-16. doi: 10.1128/mSystems.00028-16

Experimental evolution in silico: a custom-designed mathematical model for virulence evolution of Bacillus thuringiensis.

Strauß J F, Crain P, Schulenburg H, Telschow A (2016); Zoology, doi: 10.1016/j.zool.2016.03.005

WormExp: a web-based application for a Caenorhabditis elegans-specific gene expression enrichment analysis.

Yang W, Dierking K, Schulenburg H (2016); Bioinformatics, 32(6):943-945. doi: 10.1093/bioinformatics/btv667.

High innate immune specificity through diversification of C type lectin-like domain proteins in invertebrates.

Pees B, Yang W, Zarate-Potes A, Schulenburg H, Dierking K (2016); J. Innate Immunity, 8:129-142. doi: 10.1159/000441475

Ontogenic growth as the root of fundamental differences between childhood and adult cancer.

Werner B, Traulsen A, Dingli D (2016); Stem Cells., 34(3):543-50. doi: 10.1002/stem.2251

The Holobiont Imperative.

Bosch T C G and D Miller (2016); Springer New York, ISBN: 978-3-7091-1894-8

Host-parasite coevolution: Why changing population size matters.

Papkou A, Gokhale C, Traulsen A, Schulenburg H (2016); Zoology, doi: 10.1016/j.zool.2016.02.001

The cancer stem cell fraction in hierarchically organized tumors can be estimated using mathematical modeling and patient-specific treatment trajectories.

Werner B, Scott J G, Sottoriva A, Anderson A R, Traulsen A, Altrock P M (2016); Cancer Research, 76(7):1705-13, doi: 10.1158/0008-5472.CAN-15-2069

The Significance of Mutualistic Phages for Bacterial Ecology and Evolution

Obeng N, Pratama A A, Elsas J D (2016);Trends Microbiol., 24(6):440-9. doi: 10.1016/j.tim.2015.12.009

Ordering structured populations in multiplayer cooperation games.

Peña J, Wu B, Traulsen A (2016); Journal of the Royal Society, Interface / the Royal Society, 13(114):20150881. doi: 10.1098/rsif.2015.0881

Which risk scenarios can drive the emergence of costly cooperation?

Hagel K, Abou Chakra M, Bauer B, Traulsen A (2016); Scientific Reports, 6:19269. doi: 10.1038/srep19269

High instability of a nematicidal Cry toxin plasmid in Bacillus thuringiensis.

Sheppard A E, Nakad R, Saebelfeld M, Masche A C, Dierking K, Schulenburg H (2016); J.Invert.Path., 133:34-40. doi: 10.1016/j.jip.2015.11.009

Expanding our Understanding of the Seaweed Holobiont: RNA Viruses of the Red Alga Delisea pulchra.

Lachnit T, Thomas T, Steinberg P (2016); Front Microbiol., 6:1489. doi: 10.3389/fmicb.2015.01489

High Innate Immune Specificity through Diversified C-Type Lectin-Like Domain Proteins in Invertebrates.

Pees B, Yang W, Zárate-Potes A, Schulenburg H, Dierking K (2016); J Innate Immun., 8(2):129-42. doi: 10.1159/000441475

2015

Modes of migration and multilevel selection in evolutionary multiplayer games.

Pichugin Y, Gokhale C S, Garcia J, Traulsen A, Rainey P B (2015); J Theor Biol., 387:144-53. doi: 10.1016/j.jtbi.2015.09.027

Most Undirected Random Graphs Are Amplifiers of Selection for Birth-Death Dynamics, but Suppressors of Selection for Death-Birth Dynamics.

Hindersin L, Traulsen A (2015); PLoS Comput Biol., 11(11):e1004437. doi: 10.1371/journal.pcbi.1004437

Reconstructing the in vivo dynamics of hematopoietic stem cells from telomere length distributions.

Werner B, Beier F, Hummel S, Balabanov S, Lassay L, Orlikowsky T, Dingli D, Brümmendorf T m H, Traulsen A (2015); Elife., pii:e08687. doi: 10.7554/eLife.08687

When the mean is not enough: Calculating fixation time distributions in birth-death processes.

Ashcroft P, Traulsen A, Galla T (2015); Phys Rev E Stat Nonlin Soft Matter Phys., 92(4):042154. doi: 10.1103/PhysRevE.92.042154

Revisiting the age, evolutionary history and species level diversity of the genus Hydra (Cnidaria: Hydrozoa).

Schwentner M, Bosch T C (2015); Mol Phylogenet Evol., 91:41-55. doi: 10.1016/j.ympev.2015.05.013

Host-parasite coevolution in populations of constant and variable size.

Song Y, Gokhale C S, Papkou A, Schulenburg H, Traulsen A (2015); BMC Evol Biol., 15:212. doi: 10.1186/s12862-015-0462-6

Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents.

Gilbert S F, Bosch T C, Ledón-Rettig C (2015); Nat Rev Genet., 16(10):611-622. doi: 10.1038/nrg3982

Modeling evolutionary games in populations with demographic structure.

Li X Y, Giaimo S, Baudisch A, Traulsen A (2015); J Theor Biol., 380:506-15. doi: 10.1016/j.jtbi.2015.05.036

Mathematical universality and direct applicability of evolutionary games: Comment on “Universal scaling for the dilemma strength in evolutionary games”, by Z. Wang et al.

Arranz J, Traulsen A (2015); Phys Life Rev., 14:31-3. doi: 10.1016/j.plrev.2015.07.011

Stochastic game dynamics under demographic fluctuations.

Huang W, Hauert C, Traulsen A (2015); Proc Natl Acad Sci U S A., 112(29):9064-9. doi: 10.1073/pnas.1418745112

Evolutionary Transition from Pathogenicity to Commensalism: Global Regulator Mutations Mediate Fitness Gains through Virulence Attenuation.

Jansen G, Crummenerl LL, Gilbert F, Mohr T, Pfefferkorn R, Thänert R, Rosenstiel P, Schulenburg H (2015); Mol Biol Evol., 32(11) 2883-2896. doi: 10.1093/molbev/msv160

Ten years of life in compost: temporal and spatial variation of North German Caenorhabditis elegans populations.

Petersen C, Saebelfeld M, Barbosa C, Pees B, Hermann R J, Schalkowski R, Strathmann E A, Dirksen P, Schulenburg H (2015); Ecol Evol., 5(16):3250-63. doi: 10.1002/ece3.1605

Travelling at a slug’s pace: possible invertebrate vectors of Caenorhabditis nematodes.

Petersen C, Hermann R J, Barg M C, Schalkowski R, Dirksen P, Barbosa C, Schulenburg H (2015); BMC Ecol, 15:19. doi: 10.1186/s12898-015-0050-z

Partners or rivals? Strategies for the iterated prisoner’s dilemma.

Hilbe C, Traulsen A, Sigmund K (2015); Games Econ Behav., 92:41-52. doi: 10.1016/j.geb.2015.05.005

Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Fraune S, Franzenburg S, Schröder S, Augustin R, Anton-Erxleben F, Bosch TCG. (2015); ISME Journal, 9:1543–1556. doi: 10.1038/ismej.2014.239

Which games are growing bacterial populations playing?

Li XY, Pietschke C, Fraune S, Altrock PM, Bosch TC, Traulsen A (2015); J R Soc Interface., 12(108). doi: 10.1098/rsif.2015.0121

Evolutionary performance of zero-determinant strategies in multiplayer games.

Hilbe C, Wu B, Traulsen A, Nowak M A (2015); J Theor Biol., 374:115-24. doi: 10.1016/j.jtbi.2015.03.032

Host-pathogen coevolution: the selective
advantage of Bacillus thuringiensis virulence and its Cry toxin genes.

Masri L, Branca A, Sheppard AE, Papkou A, Laehnemann D, Guenther PS, Prahl S, Saebelfeld M,
Hollensteiner J, Liesegang H, Brzuszkiewicz E, Daniel R, Michiels NK, Schulte RD, Kurtz J, Rosenstiel
 P, Telschow A, Bornberg-Bauer E, Schulenburg H (2015); PLoS Biol., doi: 10.1371/journal.pbio.1002169

Using a sequential regimen to eliminate bacteria at sub-lethal antibiotic dosages.

Fuentes-Hernandez A, Plucain J, Gori F, Reding C, Peña-Miller R, Jansen G, Schulenburg H, 
Beardmore R (2015); PLoS Biol., 13(4):e1002104. doi: 10.1371/journal.pbio.1002104

Microbial ecology in Hydra: Why viruses matter.

Bosch T C G, Grasis J A, Lachnit T (2015); J Microbiol, 53(3):193-200. doi: 10.1007/s12275-015-4695-2

Why we need more ecology for genetic models like C.
elegans.

Petersen C, Dirksen P, Schulenburg H (2015); Trends Genet., 31:120-127. doi: 10.1016/j.tig.2014.12.001

Microbial ecology in Hydra: Why viruses matter.

Bosch T C, Grasis J, Lachnit T (2015); The Journal of Microbiology, 53(3):193-200. doi: 10.1007/s12275-015-4695-2

Overlapping and unique signatures in the proteomic and transcriptomic responses of the nematode Caenorhabditis elegans towards pathogenic Bacillus thuringiensis.

Yang W, Dierking K, Esser D, Tholey A, Leippe M, Rosenstiel P, Schulenburg H (2015); Dev Comp Immunol, 51:1-9. doi: 10.1016/j.dci.2015.02.010

Expanding our Understanding of the Seaweed Holobiont: RNA Viruses of the Red Alga Delisea pulchra.

Lachnit T, Thomas T, Steinberg P (2015); Frontiers in Microbiology, 6(e368). doi: 10.3389/fmicb.2015.01489

2014

How do environmental factors influence life cycles and development? An experimental framework for early-diverging metazoans.

Bosch T C, Adamska M, Augustin R, Domazet-Loso T, Foret S, Fraune S, Funayama N, Grasis J, Hamada M, Hatta M, Hobmayer B, Kawai K, Klimovich A, Manuel M, Shinzato C, Technau U, Yum S, Miller D J(2014); Bioessays., 36(12):1185-94. doi: 10.1002/bies.201400065

Cooperation and control in multiplayer social dilemmas.

Hilbe C, Wu B, Traulsen A, Nowak M A (2014); Proc Natl Acad Sci U S A., 111(46):16425-30. doi: 10.1073/pnas.1407887111

Species-specific viromes in the ancestral holobiont Hydra.

Grasis J A, Lachnit T, Anton-Erxleben F, Lim Y W, Schmieder R, Fraune S, Franzenburg S, Insua S, Machado G, Haynes M, Little M, Kimble R, Rosenstiel P, Rohwer F L, Bosch T C (2014); PLoS One., 9(10):e109952. doi: 10.1371/journal.pone.0109952

Rethinking the role of immunity: lessons from Hydra

Bosch T C G (2014); Trends Immunol., 35(10):495-502. doi: 10.1016/j.it.2014.07.008

Naturally occurring tumors in the basal metazoan Hydra.

Domazet-Lošo T, Klimovich A, Anokhin B, Anton-Erxleben F, Hamm M, Lange C, Bosch T C G (2014); Nat Communications, 5:4222. doi: 10.1038/ncomms5222

Disease-.induced modification of prey competition in eco-epidemiological models

Sieber M, Malchow H, Frank M, Hilker C (2014); Ecological Complexity, 18(2014):74–82. doi: 10.1016/j.ecocom.2013.06.002

Do-or-die life cycles and diverse post-infection resistance mechanisms limit the evolution of parasite host ranges.

Sieber M, Gudelj I (2014); Ecol Lett., 17(4):491-8. doi: 10.1111/ele.12249

Fluorescence-Based Quasicontinuous and In Situ Monitoring of Biofilm Formation Dynamics in Natural Marine Environments.

Fischer M, Friedrichs G, Lachnit T (2014); Applied and Environmental Microbiology, 80(12). doi: 10.1128/AEM.00298-14

Dispersal network structure and infection mechanism shape diversity in a coevolutionary bacteria-phage system.

Sieber M, Robb M, Forde S E, Gudelj I (2014); ISME J., 8(3):504-14. doi: 10.1038/ismej.2013.169

The prevalence of Caenorhabditis 
elegans across 1.5 years in selected North German locations: the importance of substrate
type, abiotic parameters and Caenorhabditis competitors.

Petersen C, Dirksen P, Prahl S, Strathmann E A, Schulenburg H (2014); BMC Ecol., 14:4. doi: 10.1186/1472-6785-14-4

Regulation of polyp-to-jellyfish transition in Aurelia aurita.

Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst E M, Dirksen P, Bohm A M, Hemmrich G, Sommer F, Domazet-Loso T, Klostermeier U C, Anton-Erxleben F, Rosenstiel P, Bosch T C, Khalturin K (2014); Curr Biol, 24(3):263-273. doi: 10.1016/j.cub.2013.12.003

2013

Lotka-Volterra dynamics kills the Red
Queen: population size fluctuations and associated stochasticity dramatically change host-parasite
coevolution.

Gokhale C, Papkou A, Traulsen A, Schulenburg H (2013); BMC Evolutionary Biology, 13:254. doi: 10.1186/1471-2148-13-254

The effect of population structure on the rate of evolution.

Frean M, Rainey P B, Traulsen A (2013); 
Proc. Royal Soc., 7(280):1762. doi: 10.1098/rspb.2013.0211

Gene-environment and protein degradation
signatures characterize genomic and phenotypic diversity in wild Caenorhabditis elegans populations.

Volkers R M, Snoek L B, Van Hellenberg Hubar C J V, Coopman R, Chen W, Yang W, Sterken M G, 
Schulenburg H, Braeckman B P, Kammenga J E (2013); 
BMC Biol., 13:254. doi: 10.1186/1741-7007-11-93

Sex differences in host defense interfere with parasite-mediated selection for outcrossing
during host-parasite coevolution.

Masri L, Schulte R, Timmermeyer N, Thanisch S, Crummenerl L, Jansen G, Michiels N K, Schulenburg 
H (2013);. Ecol. Lett., 16:461-466. doi: 10.1111/ele.12068

When the most potent combinations of antibiotics select for the greatest bacterial
load: the smile-frown transition.

Peña-Miller R, Laehnemann D, Jansen G, Fuentes-Hernandez A, Rosenstiel P, Schulenburg H,
 Beardmore R (2013); PLoS Biol., 11:e1001540. doi: 10.1371/journal.pbio.1001540

Bacterial colonization of Hydra hatchlings follows a robust temporal pattern.

Franzenburg S, Fraune S, Altrock P M, Künzel S, Baines J F, Traulsen A, Bosch T C G (2013); ISME J., 7(4):781-90. doi: 10.1038/ismej.2012.156

Distinct antimicrobial peptide expression determines host species-specific bacterial associations

Franzenburg S, Walter J, Künzel S, Wang J, Baines J F, Bosch T C G, Fraune S (2013); Proc Natl Acad Sci USA, 110(39):E3730-8. doi: 10.1073/pnas.1304960110

Animals in a bacterial world, a new imperative for the life sciences.

McFall-Ngai M, Hadfield M, Bosch T C G, Carey H, Domazet-Loso T, Douglas A, Dubilier N, Eberl G, Fukami T, Gilbert S, Hentschel U, King N, Kjelleberg S, Knoll A, Kremer N, Mazmanian S, Metcalf J, Nealson K, Pierce N, Rawls J, Reid A, Ruby E, Rumpho M, Sanders J, Tautz D, Wernegreen J (2013); Proc Natl Acad Sci USA, 110(9):3229-36. doi: 10.1073/pnas.1218525110

The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases.

Hornung C, Poehlein A, Haack F S, Schmidt M, Dierking K, Pohlen A, Schulenburg H, Blokesch M, Plener L, Jung K, Bonge A, Krohn-Molt I, Utpatel C, Timmermann G, Spieck E, Pommerening-Röser A, Bode E, Bode H B, Daniel R, Schmeisser C, Streit W R (2013); PLoS One, 8(2). doi: 10.1371/journal.pone.0055045

Compounds associated with algal surfaces mediate epiphytic colonization of the marine macroalga Fucus vesiculosus.

Lachnit T, Fischer M, Künzel S, Harder T (2013); FEMS Microbiology Ecology, 84(2). doi: 10.1111/1574-6941.12071

2012

The impact of random frequency-dependent mutations on the
average population fitness.

Huang W, Werner B, Traulsen A (2012); BMC Evolutionary Biology, 12:160. doi: 10.1186/1471-2148-12-160

Emergence of stable polymorphisms driven by
evolutionary games between mutants.

Huang W, Haubold B, Hauert C, Traulsen A (2012); Nat Commun., 3:919. doi: 10.1038/ncomms1930

Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans.

Fraune J, Alsheimer M, Volff JN, Busch K, Fraune S, Bosch T C G, Benavente R (2012); Proc. Natl. Acad. Sci. USA, 109:16588-16593. doi: 10.1073/pnas.1206875109

MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers.

Franzenburg S, Fraune S, Künzel S, Baines J F, Domazet-Loso T, Bosch T C G (2012); Proc Natl Acad Sci USA, 109(47):19374-9. doi: 10.1073/pnas.1213110109

FoxO is a critical regulator of stem cell maintenance and immortality in Hydra.

Boehm A M, Hemmrich G, Khalturin K, Puchert M, Anton-Erxleben F, Wittlieb J, Klostermeier U C, Rosenstiel P, Oberg H H, Bosch T C G (2012); Proc Natl Acad Sci USA, 109(48):19697-702. doi: 10.1073/pnas.1209714109

MyD88 deficient Hydra reveal an ancient function of TLR-signaling in sensing bacterial colonizers.

Franzenburg S, Fraune S, Künzel S, Baines J F, Domazet-Loso T, Bosch T C (2012); Proc Natl Acad Sci U S A., 109(47):19374-9. doi: 10.1073/pnas.1213110109

Blood system formation in the urochordate Ciona intestinalis requires the variable receptor vCRL1.

Sommer F, Awazu S, Anton-Erxleben F, Jiang D, Klimovich A V, Klimovich B V, Samoilovich M P, Satou Y, Krüss M, Gelhaus C, Kürn U, Bosch T C, Khalturin K (2012); Mol Biol Evol., 29(10): 3081-3093. doi: 10.1093/molbev/mss120

The hydra effect in predator-prey models.

Sieber M, Hilker F M (2012); J Math Biol., 64(1-2):341-60. doi: 10.1007/s00285-011-0416-6

Where simplicity meets complexity: hydra, a model for host-microbe interactions.

Augustin R, Fraune S, Franzenburg S, Bosch T C (2012); Adv Exp Med Biol., 710:71-81. doi: 10.1007/978-1-4419-5638-5_8

2011

A novel metagenomic short-chain dehydrogenase/reductase attenuates Pseudomonas aeruginosa biofilm formation and virulence in Caenorhabditis elegans.

Bijtenhoorn P, Mayerhofer H, Muller-Dieckmann J, Utpatel C, Schipper C, Hornung C, Szesny M, Grond S, Thruner A, Brzuszkiewicz E, Daniel R, Dierking K, Schulenburg H, Streit W R (2011); PLoS One, 6(10):e26278. doi: 10.1371/journal.pone.0026278.

Host-parasite local adaptation
after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis.

Schulte R D, Makus C, Hasert B, Michiels N K, Schulenburg H (2011); 
Proc. R. Soc. Lond. B, 278(1719):2832-2839. doi: 10.1098/rspb.2011.0019

rRNA-based profiling of bacteria in the axilla of healthy males suggests right-left asymmetry in bacterial activity.

Egert M, Schmidt I, Höhne H-M, Lachnit T, Schmitz R , Breves R (2011); FEMS Microbiology Ecology, 77:146-153. doi: 10.1111/j.1574-6941.2011.01097.x

Embryo protection in contemporary immunology: Why bacteria matter.

Fraune S, Augustin R, Bosch T C (2011); Commun Integr Biol., 4(4):369-72. doi: 10.4161/cib.4.4.15159

Prey, predators, parasites: intraguild predation or simpler community modules in disguise?

Sieber M, Hilker F M (2011); J Anim Ecol., 80(2):414-21. doi: 10.1111/j.1365-2656.2010.01788.x

Epibacterial community patterns on marine macroalgae are host-specific but temporally variable.

Lachnit T, Meske D, Wahl M, Harder T, Schmitz R A (2011); Environmental Microbiology, 13(3):655-65. doi: 10.1111/j.1462-2920.2010.02371.x

2010

Noise can prevent onset of chaos in spatiotemporal population dynamics.

Petrovskii S, Morozov A, Malchow H, Sieber M (2010); Eur. Phys. J. B, 78(2):253–264. doi: 10.1140/epjb/e2010-10410-8

In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

Fraune S, Augustin R, Anton-Erxleben F, Wittlieb J, Gelhaus C, Klimovich VB, Samoilovich MP, Bosch TCG (2010); Proc. Natl. Acad. Sci., 107(42):18067-18072. doi: 10.1073/pnas.1008573107

Why bacteria matter in animal development and evolution.

Fraune S,Bosch T C G (2010); Bioessays, 32(7):571-80. doi: 10.1002/bies.200900192

Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: Patterns of microfouling and antimicrobial protection.

Wahl M, Shahnaz L, Dobretsov S, Saha M, Symanowski F, David K, Lachnit T, Vasel M, Weinberger F (2010); Marine Ecology Progress Series, 411:33-48. doi: 10.3354/meps08644

Multiple reciprocal adaptations
and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite.

Schulte R D, Makus C, Hasert B, Michiels N K, Schulenburg H (2010); 
Proc. Natl. Acad. Sci. USA, 107(16):7359–7364. doi: 10.1073/pnas.1003113107

Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga.

Lachnit T, Wahl M, Harder T (2010); Biofouling, 26(3):247-55. doi: 10.1080/08927010903474189

The dynamic genome of Hydra.

Chapman J A, Kirkness E F, Simakov O, Hampson S E, Mitros T, Weinmaier T, Rattei T, Balasubramanian P G, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton G G, Viswanathan L D, Walenz B, Goodstein D M, Hellsten U, Kawashima T, Prochnik S E, Putnam N H, Shu S, Blumberg B, Dana C E, Gee L, Kibler D F, Law L, Lindgens D, Martinez D E, Peng J, Wigge P A, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang J S, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz P R, Zhang X, Aufschnaiter R, Eder M K, Gorny A K, Salvenmoser W, Heimberg A M, Wheeler B M, Peterson K J, Böttger A, Tischler P, Wolf A, Gojobori T, Remington K A, Strausberg R L, Venter J C, Technau U, Hobmayer B, Bosch T C G, Holstein T W, Fujisawa T, Bode H R, David C N, Rokhsar D S, Steele R E (2010); Nature, 464:592-6. doi: 10.1038/nature08830

Evolutionary games in the multiverse.

Gokhale J and Traulsen A (2010); Proc. Natl. Acad. Sci. USA, 107(12):5500-5504. doi: 10.1073/pnas.0912214107

How Hydra senses and destroys microbes.

Augustin R , Fraune S, Bosch T C (2010); Semin Immunol., 22(1):54-8. doi: 10.1016/j.smim.2009.11.002

Noise-induced suppression of periodic travelling waves in oscillatory reaction–diffusion systems.

Sieber M, Malchow H, Petrovskii S V (2010); The Royal Society, 466:1903–1917. doi: 10.1098/rspa.2009.0611

2009

Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice?

Jaenicke E, Fraune S, May S, Irmak P, Augustin R, Meesters C, Decker H, Zimmer M (2009); Dev Comp Immunol., 33(10):1055-63. doi: 10.1016/j.dci.2009.05.005

Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota.

Fraune S, Abe Y, Bosch T C G (2009); Environ. Microbiol., 11(9):2361-2369. doi: 10.1111/j.1462-2920.2009.01963.x

More than just orphans: are taxonomically-restricted genes important in evolution?

Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch T C (2009); Trends Genet., 25(9):404-13. doi: 10.1016/j.tig.2009.07.006

Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence.

Bosch T C, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, Zill H, Rosenstiel P, Jacobs G, Schreiber S, Leippe M, Stanisak M, Grötzinger J, Jung S, Podschun R, Bartels J, Harder J, Schröder J M (2009); Dev Comp Immunol., 33(4):559-69. doi: 10.1016/j.dci.2008.10.004

Plasticity of epithelial cell shape in response to upstream signals: a whole-organism study using transgenic Hydra.

Anton-Erxleben F, Thomas A, Wittlieb J, Fraune S, Bosch TC (2009); Zoology (Jena), 112(3):185-94. doi: 10.1016/j.zool.2008.09.002

Specific epibacterial communities on macroalgae: phylogeny matters more than habitat.

Lachnit T, Blümel M, Imhoff J F, Wahl M (2009); Aquatic Biology, 5(2):181-186. doi: 10.3354/ab00149

2008

Host-specificity of environmentally transmitted Mycoplasma-like isopod symbionts.

Fraune S, Zimmer M (2008); Environ Microbiol., 10(10):2497-504.

Analytical results for individual and group selection of any
intensity.

Traulsen A, Shoresh N, Nowak M A (2008); Bulletin of Mathematical Biology, 70:1410-1424. doi: 10.1007/s11538-008-9305-6

Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans.

Schulenburg H, Hoeppner M P, Weiner J 3rd, Bornberg-Bauer E (2008); Immunobiology., 213(3-4):237-50. doi: 10.1016/j.imbio.2007.12.004

2007

Constructive effects of environmental noise in an excitable prey-predator plankton system with infected prey.

Sieber M, Malchow H, Schimansky-Geier L (2007); Ecological complexity, 4(4):223-233. doi: 10.1016/j.ecocom.2007.06.005

Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra.

Fraune S, Bosch TCG (2007); Proc Natl Acad Sci USA, 104(32):13146-51. doi: 10.1073/pnas.0703375104

Via freedom to coercion: The 
emergence of costly punishment.

Hauert C, Traulsen A, Brandt H, Nowak M A, Sigmund K (2007); Science, 316(5833):1905-1907. doi: 10.1126/science.1141588

Allorecognition in urochordates: identification of a highly variable complement receptor-like protein expressed in follicle cells of Ciona.

Kurn U, Sommer F, Hemmrich G, Bosch T C, Khalturin K (2007); Dev Comp Immunol., 31(4):360-371. doi: 10.1016/j.dci.2006.06.008

2006

In the urochordate Ciona intestinalis zona pellucida domain proteins vary among individuals.

Kurn U, Sommer F, Bosch T C, Khalturin K (2006); Developmental and comparative immunology, 31(12): 1242-1254. doi: 10.1016/j.dci.2007.03.011

Coevolutionary dynamics in large, but finite populations.

Traulsen A, Claussen J C, Hauert C (2006); 
Phys. Rev., 95:23870. doi: 10.1103/PhysRevLett.95.238701

Evolution of cooperation by multi-level selection.

Traulsen A, Nowak M A (2006); 
Proc. Natl. Acad. Sci. USA, 103(29):10952–10955. doi: 10.1073/pnas.0602530103

Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis.

Wittlieb J, Khalturin K, Lohmann J, Anton-Erxleben F, Bosch T C G (2006); Proc. Natl. Acad. Sci. USA, 103(16):6208-6211. doi: 10.1073/pnas.0510163103