Funding and projects

Convergent evolution of immunological tolerance in female and male pregnancy 

DFG Project - PI: Olivia Roth

 

Unravelling tripartite species co-evolution under environmental change: can prophages accelerate bacterial virulence evolution

DFG Priority Programme - Rapid evolutionary Adaptation - Phase II - PI: Olivia Roth

 

 

MALEPREG: Male pregnancy - unravelling the coevolution of parental Investment and immune defence 

ERC Starting Grant - PI: Olivia Roth

 

DFG Research Training Group for Translational Evolutionary Research

DFG Research Training group TransEvo - Speaker: Hinrich Schulenburg

 

 

Coevolution of pregnancy and immune defence

Pregnancy is among the most impressive cases of convergent evolution. To understand how and why pregnancy evolved so many times independently, we need to identify selection regimes and compare the underlying genomic basis. The unique male pregnancy in pipefishes and seahorses is optimally suited to assess pregnancy evolution, as pregnancy is displayed on a gradient, with several transitions in closely related species. Using comparative genomics, we discovered that male pregnancy coevolved with a  functional loss of one arm of the adaptive immune system, the Major Histocompatibility Complex II (MHC II) (Roth et al., 2020, Haase et al., 2013). Our results suggest that evolution of female and male pregnancy relies on the co-option of similar genes and pathways (Roth et al., 2020).

 

We are analysing male pregnancy evolution and assess the flexibility of the immune system in marine teleosts (Roth et al., 2020). We assess whether male pregnancy coevolved with immunological tolerance of the non-self embryo and thus affected self vs. non-self-recognition, using tissue transplant experiments, transcriptomics and comparative genomics of de novo sequenced genomes of syngnathid species. To unravel convergent pregnancy evolution, we compare genes used in female and male pregnancy, using transcriptomics and genomics approaches. We, further, explore whether the microbial communities in the brood pouch of syngnathids have coevolved with the extent of male pregnancy and the rearrangement of the immune system (Beemelmanns et al., 2019). We aim to use genome-wide selection analyses to identify the key genes involved in pregnancy evolution, the functions of which will be assessed over CRISPR/cas9 technology.

 

People involved:

 

Olivia Roth

Ralf Schneider

Arseny Dubin

Isabel Tanger

Jamie Parker

Kim Wagner

Silke Mareike Marten

Johannes Hasse

 

 

Collaborator:

 

Sissel Jentoft

 

 

Cited literature:

 

Beemelmanns A, Poirier M, Bayer T, Kuenzle S & Roth O. 2019. Microbial embryonal colonization during pipefish male pregnancy. Scientific Reports 9: 3.

 

Haase D, Roth O, Kalbe M, Schmiedeskamp G, Scharsack JP, Rosenstiel B & Reusch TBH (2013). Functional absence of MHC class II mediated immunity in pipefish Syngnathus typhleBiology Letters 9.

 

Roth O, Solbakken MH, Torresen OK, Matschiner M, Baalsrund HT, Hoff SNK, Brieuc MSO, Haase D, Hanel R, Reusch TBH & Jentoft S. 2020. Evolution of male pregnancy associated with remodelling of canonical vertebrate immunity in seahorses and pipefishes. PNAS 117: 9431-9439.

 

 

 

Sex, immunity and life history

The evolution of male pregnancy in syngnathids challenges concepts in evolutionary biology, as egg production and parental investment, two traits that are usually intermingled in the female sex, are here disentangled. This makes these fish a great model system to investigate how parental investment drives sexual dimorphism. Not only maternal but also paternal immune status (Beemelmanns & Roth, 2017) affect the offspring immune response via trans-generational immune priming (TGIP) (Roth & Landis, 2017, Roth et al., 2012, Beemelmanns & Roth, 2016). Males in sex-role reversed species are proposed to invest more into their offspring than males in conventional sex-role species, including an increased investment in immune protection, as confirmed for male pregnant syngnathids (Roth et al., 2011, Keller & Roth, 2020).

 

Sex-specific resource allocation towards the distinct life-history traits has a direct impact on adult sex ratio (Revathi Venkanteswaran et al., 2020). We aim to validate this in the field, assessing the impact of parental investment, immune defence and ornamentation on adult sex ratio. We further want to study the evolution of sexual antagonistic conflict and sexual dimorphism by comparing closely related syngnathid species along the paternal investment and mating system gradient, using genomics and experimental approaches in collaboration with Astrid Böhne (Museum König, Bonn). Finally, in the Research Training Group Translational Evolutionary Research, we collaborate with Almut Nebel (CAU Kiel) to assess the sex-specific link between fertility, pregnancy and longevity, combining genomic analyses of the relevant life-history traits and their functional characterization in sex-role reversed syngnathids.

 

People involved:

 

Olivia Roth

Arseny Dubin

Isabel Tanger

Freya Pappert

 

Collaborators:

 

Astrid Böhne

Almut Nebel

 

 

Cited literature:

 

Beemelmanns A & Roth O.2017. Grandparental immune priming in the pipefish Syngnathus typhleBMC Evolutionary Biology 17: 44.

 

Roth O & Landis SH. 2017. Trans-generational plasticity in response to immune challenge is constrained by heat stress,Evolutionary Applications 10: 514-528.

 

Beemelmanns A & Roth O (2016). Biparental immune priming in the pipefish Syngnathus typhleZoology 119: 262 - 272.

 

Roth O, Klein V, Beemelmanns A, Scharsack JP & Reusch TBH (2012). Male pregnancy and bi-parental immune priming. American Naturalist, 180: 802-814.

 

Roth O, Scharsack, JP, Keller I & Reusch TBH (2011). Bateman´s principle and immunity in a sex-role reversed pipefish. Journal of Evolutionary Biology 24: 1410 - 1420.

 

Tanger IS & Roth O. 2020. Parental investment and immune dynamics in sex-role reversed pipefishes. PLOS one 15: e0228974.

 

 

Tripartite species coevolution

Host-pathogen interactions are ideal to track rapid adaptation and counter-adaptation on contemporary time scales. Temperate bacteriophages integrate into the bacterial genome, and can turn a harmless bacterium into a deadly disease by providing virulence genes. A number of human infectious diseases, e.g. diphtheria & cholera, result from such tripartite interactions, involving the human host, a bacterium, and its phage. With our marine model system (pipefish, opportunistic Vibrio bacteria and their temperate phages), we study patterns and dynamics of rapid virulence evolution. We found strong bacteria genotype by bacteriophage genotype interactions and that bacteria virulence towards pipefish is correlated with Vibrio susceptibility to phages (Wendling et al., 2018, Wendling et al., 2017). We generated high quality reference genomes of nine V. alginolyticus species and revealed that prophages, transposable elements, and plasmids play a major role in the phylogenetic diversity and niche adaptation of this species (Chibani et al., 2020, Chibani et al., 2017). With experimental evolution, we demonstrated that bacteria rapidly gained resistance against phages. Oceanic environmental change (i.e., a drop of salinity levels as predicted for the Baltic Sea) impacted the phage bacteria coevolution.

 

Now we will investigate how the co-evolution between phage and bacterium is impaired by the immune system and the microbiota of the eukaryotic host. To reach this goal, we will run infection experiments and conduct serial passage experiments to unravel phage-bacteria coevolution inside the eukaryotic host.

 

 

People involved:

 

Olivia Roth

Jelena Rajkov

Silke Mareike Marten

 

 

Collaborator:

 

Carolin Wendling

 

 

Cited literature:

 

Wendling CC, Piecyk A, Refardt D, Chibani C, Hertel R, Liesegang H, Bunk B & Roth O. 2017. Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria. BMC Evolutionary Biology 17: 98.

 

Wendling CC, Göhlich H & Roth O. 2018. The structure of temperate phage-bacteria infection networks changes with the phylogenetic distance of the host bacteria. Biology Letters 14:20180320.

 

Chibani CM, Liesegang H, Roth O & Wendling CC. 2020. Genomic variation among closely related Vibrio alginolyticus strains is located on mobile genetic elements. BMC Genomics 21:354.